Diffusion-tensor MR imaging of gray and white matter development during normal human brain maturation.

BACKGROUND AND PURPOSE Conventional MR imaging findings of human brain development are thought to result from decreasing water content, increasing macromolecular concentration, and myelination. We use diffusion-tensor MR imaging to test theoretical models that incorporate hypotheses regarding how these maturational processes influence water diffusion in developing gray and white matter. METHODS Experimental data were derived from diffusion-tensor imaging of 167 participants, ages 31 gestational weeks to 11 postnatal years. An isotropic diffusion model was applied to the gray matter of the basal ganglia and thalamus. A model that assumes changes in the magnitude of diffusion while maintaining cylindrically symmetric anisotropy was applied to the white matter of the corpus callosum and internal capsule. Deviations of the diffusion tensor from the ideal model predictions, due to measurement noise, were estimated by using Monte Carlo simulations. RESULTS Developing gray matter of the basal ganglia and developing white matter of the internal capsule and corpus callosum largely conformed to theory, with only small departures from model predictions in older children. However, data from the thalamus substantially diverged from predicted values, with progressively larger deviations from the model with increasing participant age. CONCLUSION Changes in water diffusion during maturation of central gray and white matter structures can largely be explained by theoretical models incorporating simple assumptions regarding the influence of brain water content and myelination, although deviations from theory increase as the brain matures. Diffusion-tensor MR imaging is a powerful method for studying the process of brain development, with both scientific and clinical applications.

[1]  J. Dobbing,et al.  Quantitative growth and development of human brain , 1973, Archives of disease in childhood.

[2]  D. Norman,et al.  Normal maturation of the neonatal and infant brain: MR imaging at 1.5 T. , 1988, Radiology.

[3]  J. Pearlman,et al.  CSF‐suppressed quantitative single‐shot diffusion imaging , 1991, Magnetic resonance in medicine.

[4]  C. Beaulieu,et al.  Determinants of anisotropic water diffusion in nerves , 1994, Magnetic resonance in medicine.

[5]  T Nakagawa,et al.  Diffusional anisotropy of the human brain assessed with diffusion-weighted MR: relation with normal brain development and aging. , 1994, AJNR. American journal of neuroradiology.

[6]  J. Kucharczyk,et al.  Identification of “Premyelination” by Diffusion‐Weighted MRI , 1995, Journal of computer assisted tomography.

[7]  P. Basser,et al.  Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. , 1996, Journal of magnetic resonance. Series B.

[8]  E. Akbudak,et al.  Encoding of anisotropic diffusion with tetrahedral gradients: A general mathematical diffusion formalism and experimental results , 1996, Magnetic resonance in medicine.

[9]  P. Basser,et al.  Diffusion tensor MR imaging of the human brain. , 1996, Radiology.

[10]  M. Bastin,et al.  A theoretical study of the effect of experimental noise on the measurement of anisotropy in diffusion imaging. , 1998, Magnetic resonance imaging.

[11]  S. Maier,et al.  Microstructural Development of Human Newborn Cerebral White Matter Assessed in Vivo by Diffusion Tensor Magnetic Resonance Imaging , 1998, Pediatric Research.

[12]  C. Beaulieu,et al.  Multicomponent water proton transverse relaxation and T2-discriminated water diffusion in myelinated and nonmyelinated nerve. , 1998, Magnetic resonance imaging.

[13]  U. Mödder,et al.  Age-dependent changes in magnetization transfer contrast of white matter in the pediatric brain. , 1998, AJNR. American journal of neuroradiology.

[14]  A. Elster,et al.  Calculation of apparent diffusion coefficients (ADCs) in brain using two-point and six-point methods. , 1998, Journal of computer assisted tomography.

[15]  A. Snyder,et al.  Normal brain in human newborns: apparent diffusion coefficient and diffusion anisotropy measured by using diffusion tensor MR imaging. , 1998, Radiology.

[16]  T. L. Davis,et al.  Human acute cerebral ischemia: detection of changes in water diffusion anisotropy by using MR imaging. , 1999, Radiology.

[17]  G. Barker,et al.  Diffusion tensor imaging of lesions and normal-appearing white matter in multiple sclerosis , 1999, Neurology.

[18]  T. Ptak,et al.  Investigation of apparent diffusion coefficient and diffusion tensor anisotrophy in acute and chronic multiple sclerosis lesions. , 1999, AJNR. American journal of neuroradiology.

[19]  A. Snyder,et al.  Quantitative diffusion-tensor anisotropy brain MR imaging: normative human data and anatomic analysis. , 1999, Radiology.

[20]  R. A. Zimmerman,et al.  Changes in brain water diffusion during childhood , 1999, Neuroradiology.

[21]  K. Lim,et al.  Age‐related decline in brain white matter anisotropy measured with spatially corrected echo‐planar diffusion tensor imaging , 2000, Magnetic resonance in medicine.

[22]  V. Wedeen,et al.  Fiber crossing in human brain depicted with diffusion tensor MR imaging. , 2000, Radiology.

[23]  M E Bastin,et al.  Selecting an appropriate anisotropy index for displaying diffusion tensor imaging data with improved contrast and sensitivity , 2000, Magnetic resonance in medicine.

[24]  J. Kucharczyk,et al.  Visualization of nonstructural changes in early white matter development on diffusion-weighted MR images: evidence supporting premyelination anisotropy. , 2001, AJNR. American journal of neuroradiology.

[25]  R. McKinstry,et al.  Reversible posterior leukoencephalopathy syndrome: evaluation with diffusion-tensor MR imaging. , 2001, Radiology.

[26]  M Hedehus,et al.  Diffusion-tensor MR imaging at 1.5 and 3.0 T: initial observations. , 2001, Radiology.

[27]  J. Shimony,et al.  Normal brain maturation during childhood: developmental trends characterized with diffusion-tensor MR imaging. , 2001, Radiology.

[28]  D. Norris The effects of microscopic tissue parameters on the diffusion weighted magnetic resonance imaging experiment , 2001, NMR in biomedicine.