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White Matter Changes of Neurite Density and Fiber Orientation Dispersion during Human Brain Maturation.

Chang YS, Owen JP, Pojman NJ, Thieu T, Bukshpun P, Wakahiro ML, Berman JI, Roberts TP, Nagarajan SS, Sherr EH, Mukherjee P - PLoS ONE (2015)

Bottom Line: Our results suggest that the rise of FA during the first two decades of life is dominated by increasing NDI, while the fall in FA after the fourth decade is driven by the exponential rise of ODI that overcomes the slower increases of NDI.Using partial least squares regression, we further demonstrate that NODDI better predicts chronological age than DTI.Our results support the conclusion that NODDI reveals biologically specific characteristics of brain development that are more closely linked to the microstructural features of white matter than are the empirical metrics provided by DTI.

View Article: PubMed Central - PubMed

Affiliation: Department of Radiology and Biomedical Imaging, University of California San Francisco, San Francisco, California, United States of America.

ABSTRACT
Diffusion tensor imaging (DTI) studies of human brain development have consistently shown widespread, but nonlinear increases in white matter anisotropy through childhood, adolescence, and into adulthood. However, despite its sensitivity to changes in tissue microstructure, DTI lacks the specificity to disentangle distinct microstructural features of white and gray matter. Neurite orientation dispersion and density imaging (NODDI) is a recently proposed multi-compartment biophysical model of brain microstructure that can estimate non-collinear properties of white matter, such as neurite orientation dispersion index (ODI) and neurite density index (NDI). In this study, we apply NODDI to 66 healthy controls aged 7-63 years to investigate changes of ODI and NDI with brain maturation, with comparison to standard DTI metrics. Using both region-of-interest and voxel-wise analyses, we find that NDI exhibits striking increases over the studied age range following a logarithmic growth pattern, while ODI rises following an exponential growth pattern. This novel finding is consistent with well-established age-related changes of FA over the lifespan that show growth during childhood and adolescence, plateau during early adulthood, and accelerating decay after the fourth decade of life. Our results suggest that the rise of FA during the first two decades of life is dominated by increasing NDI, while the fall in FA after the fourth decade is driven by the exponential rise of ODI that overcomes the slower increases of NDI. Using partial least squares regression, we further demonstrate that NODDI better predicts chronological age than DTI. Finally, we show excellent test-retest reliability of NODDI metrics, with coefficients of variation below 5% in all measured regions of interest. Our results support the conclusion that NODDI reveals biologically specific characteristics of brain development that are more closely linked to the microstructural features of white matter than are the empirical metrics provided by DTI.

No MeSH data available.


Related in: MedlinePlus

Subject FA, ODI, and NDI age trajectories in each group of JHU tracts (excepting cerebellar tracts): projection (non-brainstem, blue), association (red), callosal (green), limbic (magenta), projection (brainstem, cyan).Shaded regions represent 95% confidence intervals.
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pone.0123656.g003: Subject FA, ODI, and NDI age trajectories in each group of JHU tracts (excepting cerebellar tracts): projection (non-brainstem, blue), association (red), callosal (green), limbic (magenta), projection (brainstem, cyan).Shaded regions represent 95% confidence intervals.

Mentions: Fig 3 reveals that, of the JHU tracts, the callosal tracts demonstrate the highest values of FA and the lowest values of ODI. The brainstem projection tracts have the highest values of NDI, with callosal and non-brainstem projection tracts also showing high values of NDI. The association and limbic tracts have the lowest values of FA, highest values of ODI, and lowest values of NDI (Fig 3). Table 6 shows that the brainstem projection tracts demonstrate a higher rate of exponential growth in ODI (higher b2 in eq. 1) relative to the other JHU tract groups: non-brainstem projection, association, limbic, callosal, and cerebellar. The brainstem projection tracts and limbic tracts show a higher rate of logarithmic growth in NDI relative to the other JHU tract groups, while the callosal and association tracts show a lower rate of logarithmic growth in NDI relative to the other JHU tract groups.


White Matter Changes of Neurite Density and Fiber Orientation Dispersion during Human Brain Maturation.

Chang YS, Owen JP, Pojman NJ, Thieu T, Bukshpun P, Wakahiro ML, Berman JI, Roberts TP, Nagarajan SS, Sherr EH, Mukherjee P - PLoS ONE (2015)

Subject FA, ODI, and NDI age trajectories in each group of JHU tracts (excepting cerebellar tracts): projection (non-brainstem, blue), association (red), callosal (green), limbic (magenta), projection (brainstem, cyan).Shaded regions represent 95% confidence intervals.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4482659&req=5

pone.0123656.g003: Subject FA, ODI, and NDI age trajectories in each group of JHU tracts (excepting cerebellar tracts): projection (non-brainstem, blue), association (red), callosal (green), limbic (magenta), projection (brainstem, cyan).Shaded regions represent 95% confidence intervals.
Mentions: Fig 3 reveals that, of the JHU tracts, the callosal tracts demonstrate the highest values of FA and the lowest values of ODI. The brainstem projection tracts have the highest values of NDI, with callosal and non-brainstem projection tracts also showing high values of NDI. The association and limbic tracts have the lowest values of FA, highest values of ODI, and lowest values of NDI (Fig 3). Table 6 shows that the brainstem projection tracts demonstrate a higher rate of exponential growth in ODI (higher b2 in eq. 1) relative to the other JHU tract groups: non-brainstem projection, association, limbic, callosal, and cerebellar. The brainstem projection tracts and limbic tracts show a higher rate of logarithmic growth in NDI relative to the other JHU tract groups, while the callosal and association tracts show a lower rate of logarithmic growth in NDI relative to the other JHU tract groups.

Bottom Line: Our results suggest that the rise of FA during the first two decades of life is dominated by increasing NDI, while the fall in FA after the fourth decade is driven by the exponential rise of ODI that overcomes the slower increases of NDI.Using partial least squares regression, we further demonstrate that NODDI better predicts chronological age than DTI.Our results support the conclusion that NODDI reveals biologically specific characteristics of brain development that are more closely linked to the microstructural features of white matter than are the empirical metrics provided by DTI.

View Article: PubMed Central - PubMed

Affiliation: Department of Radiology and Biomedical Imaging, University of California San Francisco, San Francisco, California, United States of America.

ABSTRACT
Diffusion tensor imaging (DTI) studies of human brain development have consistently shown widespread, but nonlinear increases in white matter anisotropy through childhood, adolescence, and into adulthood. However, despite its sensitivity to changes in tissue microstructure, DTI lacks the specificity to disentangle distinct microstructural features of white and gray matter. Neurite orientation dispersion and density imaging (NODDI) is a recently proposed multi-compartment biophysical model of brain microstructure that can estimate non-collinear properties of white matter, such as neurite orientation dispersion index (ODI) and neurite density index (NDI). In this study, we apply NODDI to 66 healthy controls aged 7-63 years to investigate changes of ODI and NDI with brain maturation, with comparison to standard DTI metrics. Using both region-of-interest and voxel-wise analyses, we find that NDI exhibits striking increases over the studied age range following a logarithmic growth pattern, while ODI rises following an exponential growth pattern. This novel finding is consistent with well-established age-related changes of FA over the lifespan that show growth during childhood and adolescence, plateau during early adulthood, and accelerating decay after the fourth decade of life. Our results suggest that the rise of FA during the first two decades of life is dominated by increasing NDI, while the fall in FA after the fourth decade is driven by the exponential rise of ODI that overcomes the slower increases of NDI. Using partial least squares regression, we further demonstrate that NODDI better predicts chronological age than DTI. Finally, we show excellent test-retest reliability of NODDI metrics, with coefficients of variation below 5% in all measured regions of interest. Our results support the conclusion that NODDI reveals biologically specific characteristics of brain development that are more closely linked to the microstructural features of white matter than are the empirical metrics provided by DTI.

No MeSH data available.


Related in: MedlinePlus