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Exploring the role of white matter connectivity in cortex maturation

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  • Cecilia L Friedrichs-Maeder
  • Alessandra Griffa
  • Juliane Schneider
  • Petra Susan Hüppi
  • Anita Truttmann
  • Patric Hagmann

Abstract

The maturation of the cortical gray matter (GM) and white matter (WM) are described as sequential processes following multiple, but distinct rules. However, neither the mechanisms driving brain maturation processes, nor the relationship between GM and WM maturation are well understood. Here we use connectomics and two MRI measures reflecting maturation related changes in cerebral microstructure, namely the Apparent Diffusion Coefficient (ADC) and the T1 relaxation time (T1), to study brain development. We report that the advancement of GM and WM maturation are inter-related and depend on the underlying brain connectivity architecture. Particularly, GM regions and their incident WM connections show corresponding maturation levels, which is also observed for GM regions connected through a WM tract. Based on these observations, we propose a simple computational model supporting a key role for the connectome in propagating maturation signals sequentially from external stimuli, through primary sensory structures to higher order functional cortices.

Suggested Citation

  • Cecilia L Friedrichs-Maeder & Alessandra Griffa & Juliane Schneider & Petra Susan Hüppi & Anita Truttmann & Patric Hagmann, 2017. "Exploring the role of white matter connectivity in cortex maturation," PLOS ONE, Public Library of Science, vol. 12(5), pages 1-18, May.
  • Handle: RePEc:plo:pone00:0177466
    DOI: 10.1371/journal.pone.0177466
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    1. Laurie von Melchner & Sarah L. Pallas & Mriganka Sur, 2000. "Visual behaviour mediated by retinal projections directed to the auditory pathway," Nature, Nature, vol. 404(6780), pages 871-876, April.
    2. David C. Van Essen, 1997. "A tension-based theory of morphogenesis and compact wiring in the central nervous system," Nature, Nature, vol. 385(6614), pages 313-318, January.
    3. Ho Ko & Lee Cossell & Chiara Baragli & Jan Antolik & Claudia Clopath & Sonja B. Hofer & Thomas D. Mrsic-Flogel, 2013. "The emergence of functional microcircuits in visual cortex," Nature, Nature, vol. 496(7443), pages 96-100, April.
    4. Robert A. Barton & Paul H. Harvey, 2000. "Mosaic evolution of brain structure in mammals," Nature, Nature, vol. 405(6790), pages 1055-1058, June.
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