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Diffusion-Tensor MR Imaging of Gray and White Matter Development during Normal Human Brain Maturation

Pratik Mukherjeea, Jeffrey H. Millera, Joshua S. Shimonya, Joseph V. Philipa, Deepika Nehraa, Abraham Z. Snydera, Thomas E. Conturoa, Jeffrey J. Neilb and Robert C. McKinstrya

a Mallinckrodt Institute of Radiology, St. Louis Children’s Hospital, Washington University Medical Center, St. Louis, MO
b Division of Pediatric Neurology, St. Louis Children’s Hospital, Washington University Medical Center, St. Louis, MO



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  		FIG 1. Region of interest placement is illustrated on a transverse diffusion anisotropy (A{sigma}) image obtained through the level of the basal ganglia in a 1-year-old child. Diffusion anisotropy is computed from a single shot echo-planar diffusion-tensor sequence: 3000/97.4/1 (TR/TE/number of excitations), using four tetrahedrally oriented diffusion gradients (b = 1012.4 s/mm2) and three orthogonally oriented diffusion gradients (b = 337.5 s/mm2). Regions of interest in gray matter are marked as white ellipses, and regions of interest in white matter are marked as black ellipses. Values from the left and right regions of interest were averaged. 1, head of the caudate nucleus; 2, lentiform nucleus; 3, posterior limb of the internal capsule; 4, thalamus; 5, splenium of the corpus callosum.



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  		FIG 2. Decrease in the eigenvalues of the diffusion tensor during normal brain maturation is illustrated in five participants ranging in age from 31 gestational weeks (preterm) to 6 postnatal years. Diffusion-tensor imaging parameters are as in Figure 1, except for the preterm neonate, for whom the parameters were 3000/106/1 with four tetrahedrally oriented diffusion gradients (b = 800 s/mm2) and three orthogonally oriented diffusion gradients (b = 340 s/mm2). All images are transverse sections obtained at the level of the basal ganglia. All images are displayed with identical window and level settings to allow direct comparison of signal intensity across participants. The eigenvalues are rotationally invariant measures of the rate of water diffusion along each of the three principal axes of the diffusion tensor at each MR imaging voxel. {lambda}min (top row) is the eigenvalue with the smallest magnitude, {lambda}int (middle row) has intermediate values, and {lambda}max (bottom row) has the greatest magnitude.



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  		FIG 3. The signal-to-noise ratio of diffusion-tensor imaging decreases with brain maturation.

A, Noise in the diffusion-weighted images is age-independent. In 20 participants, the noise is calculated as the SD of pixel values in an air-filled region of interest outside the brain in the b = 337.5 s/mm2 diffusion-weighted images (see Methods). The postconceptional age of each participant is the estimated gestational age added to the postnatal age. The data are fit with linear regression. The Pearson correlation coefficient of the noise with postconceptional age is 0.23, which is not statistically significant (P > .3).

B, SNR in diffusion-weighted imaging declines steeply during the first 2 years of postnatal life in the white matter of the posterior limb of the internal capsule. SNR is the quotient of signal intensity divided by noise. The signal intensity is obtained from regions of interest within the brain on b = 337.5 s/mm2 diffusion-weighted images. The data are fit with a function (equation 8 in Methods) that defines the theoretical relationship between SNR and participant age. Vertical dashed line indicates the age of normal term birth: 40 gestational weeks.

C, SNR in diffusion-weighted imaging declines steeply during the first 2 years of postnatal life in the gray matter of the lentiform nucleus. Vertical dashed line indicates the age of normal term birth: 40 gestational weeks.



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  		FIG 4. Maturational decreases of the three diffusion tensor eigenvalues ({lambda}max, {lambda}int, {lambda}min) in the gray matter of the lentiform nucleus and the gray matter of the head of the caudate nucleus for 161 participants of postconceptional ages 7 months to 12 years. Vertical dashed line indicates age of normal term birth: 40 gestational weeks. Solid lines through data are theoretical predictions for the age-varying values of {lambda}max (top line), {lambda}int (middle line), and {lambda}min (bottom line) from Monte Carlo simulation of a spherical diffusion model, to which the age-dependent parameters and SNR are given as input (see Methods for details of the theoretical model).

A, Gray matter of the lentiform nucleus. Values of {lambda}max (open inverted triangles), {lambda}int (closed circles), and {lambda}min (open squares) are in 10-3 mm2/s.

B, Gray matter of the lentiform nucleus. Each eigenvalue is expressed in terms of its fraction of the trace of the diffusion tensor Trace(D), where Trace(D) is the sum of the three eigenvalues.

C, Gray matter of the head of the caudate nucleus. Values of {lambda}max (open inverted triangles), {lambda}int (closed circles), and {lambda}min (open squares) are in 10-3 mm2/s.

D, Gray matter of the head of the caudate nucleus. Each eigenvalue is expressed in terms of its fraction of the trace of the diffusion tensor Trace(D), where Trace(D) is the sum of the three eigenvalues.



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  		FIG 5. Maturational decreases of the three diffusion tensor eigenvalues ({lambda}max, {lambda}int, {lambda}min) in the white matter of the splenium of the corpus callosum and the white matter of the posterior limb of the internal capsule for 161 participants of postconceptional ages 7 months to 12 years. Vertical dashed line indicates age of normal term birth: 40 gestational weeks. Dashed line through the {lambda}max data represents an empirical fit to a biexponential function. Solid lines through {lambda}int data (top solid line) and {lambda}min data (bottom solid line) are theoretical predictions for their age-varying values from Monte Carlo simulation of a cylindrical diffusion model, in which the age-dependent parameters , {lambda}max, and SNR are given as input (see Methods for details of the theoretical model).

A, White matter of the splenium of the corpus callosum. Values of {lambda}max (open inverted triangles), {lambda}int (closed circles), and {lambda}min (open squares) are in 10-3 mm2/s.

B, White matter of the splenium of the corpus callosum. Each eigenvalue is expressed in terms of its fraction of the trace of the diffusion tensor Trace(D), where Trace(D) is the sum of the three eigenvalues.

C, White matter of the posterior limb of the internal capsule. Values of {lambda}max (open inverted triangles), {lambda}int (closed circles), and {lambda}min (open squares) are in 10-3 mm2/s.

D, White matter of the posterior limb of the internal capsule. Each eigenvalue is expressed in terms of its fraction of the trace of the diffusion tensor Trace(D), where Trace(D) is the sum of the three eigenvalues.



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  		FIG 6. Maturational decreases of the three diffusion tensor eigenvalues ({lambda}max, {lambda}int, {lambda}min) in the thalamus for 161 participants of postconceptional ages 7 months to 12 years. Vertical dashed line indicates age of normal term birth: 40 gestational weeks. Solid lines through data are theoretical predictions for the age-varying values of {lambda}max (top line), {lambda}int (middle line), and {lambda}min (bottom line) from Monte Carlo simulation of a spherical diffusion model, to which the age-dependent parameters and SNR are given as input (see Methods for details of the theoretical model).

A, Values of {lambda}max (open inverted triangles), {lambda}int (closed circles), and {lambda}min (open squares) are in 10-3 mm2/s.

B, Each eigenvalue is expressed in terms of its fraction of the trace of the diffusion tensor Trace(D), where Trace(D) is the sum of the three eigenvalues.





Copyright © 2009 by the American Society of Neuroradiology. Print ISSN: 0195-6108 Online ISSN: 1936-959X