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Cited by 119Advanced Neuroimaging Techniques and ApplicationsDementia and Cognitive Impairment ResearchAlzheimer's disease research and treatments

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Multiple Indices of Diffusion Identifies White Matter Damage in Mild Cognitive Impairment and Alzheimer’s Disease

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O'Dwyer, Laurence, Lamberton, Franck, Bokde, Arun L. W., Ewers, Michael, Faluyi, Yetunde O., Tanner, Colby, Mazoyer, Bernard, O'Neill, Des, Bartley, Máiréad, Collins, D. Rónán, Coughlan, Tara, Prvulovic, David, Hampel, Harald·2011·PLoS ONE
DOI 10.1371/journal.pone.0021745PMC PMC3128090
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Abstract

The study of multiple indices of diffusion, including axial (DA), radial (DR) and mean diffusion (MD), as well as fractional anisotropy (FA), enables WM damage in Alzheimer's disease (AD) to be assessed in detail. Here, tract-based spatial statistics (TBSS) were performed on scans of 40 healthy elders, 19 non-amnestic MCI (MCIna) subjects, 14 amnestic MCI (MCIa) subjects and 9 AD patients. Significantly higher DA was found in MCIna subjects compared to healthy elders in the right posterior cingulum/precuneus. Significantly higher DA was also found in MCIa subjects compared to healthy elders in the left prefrontal cortex, particularly in the forceps minor and uncinate fasciculus. In the MCIa versus MCIna comparison, significantly higher DA was found in large areas of the left prefrontal cortex. For AD patients, the overlap of FA and DR changes and the overlap of FA and MD changes were seen in temporal, parietal and frontal lobes, as well as the corpus callosum and fornix. Analysis of differences between the AD versus MCIna, and AD versus MCIa contrasts, highlighted regions that are increasingly compromised in more severe disease stages. Microstructural damage independent of gross tissue loss was widespread in later disease stages. Our findings suggest a scheme where WM damage begins in the core memory network of the temporal lobe, cingulum and prefrontal regions, and spreads beyond these regions in later stages. DA and MD indices were most sensitive at detecting early changes in MCIa.

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Crossref · 10.1371/journal.pone.0021745

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Figures

Figure 1 Diffusional changes in MCI subjects for FA and MD. (a) Significantly higher FA in MCIna relative to controls is shown in green. (b) Significantly higher MD in MCIa relative to controls is shown in red.
Figure 1 Diffusional changes in MCI subjects for FA and MD. (a) Significantly higher FA in MCIna relative to controls is shown in green. (b) Significantly higher MD in MCIa relative to controls is shown in red.CC BY · PubMed Central
Figure 2 DA changes in MCIna and MCIa subjects. (a) Significantly higher DA in MCIa relative to MCIna. These significant changes are found in the left hemisphere in frontal regions. (b) Significantly higher DA in MCIa relative to control (red). These significant changes are also found in the left hemisphere in frontal regions. (c) Significantly higher DA in MCIna relative to control (blue). These significant changes are found in the right hemisphere in the parietal lobe.
Figure 2 DA changes in MCIna and MCIa subjects. (a) Significantly higher DA in MCIa relative to MCIna. These significant changes are found in the left hemisphere in frontal regions. (b) Significantly higher DA in MCIa relative to control (red). These significant changes are also found in the left hemisphere in frontal regions. (c) Significantly higher DA in MCIna relative to control (blue). These significant changes are found in the right hemisphere in the parietal lobe.CC BY · PubMed Central
Figure 3 Differences between AD and control subjects for all indices. (a) MD diffusivity, (b) DR diffusivity, (c) DA diffusivity, (d) FA diffusivity. For each index a three dimensional model of the significant changes are shown for the left and right hemispheres in the upper panels. In the lower panels, an axial slice and a sagittal slice show specific changes located at the level of the slice.
Figure 3 Differences between AD and control subjects for all indices. (a) MD diffusivity, (b) DR diffusivity, (c) DA diffusivity, (d) FA diffusivity. For each index a three dimensional model of the significant changes are shown for the left and right hemispheres in the upper panels. In the lower panels, an axial slice and a sagittal slice show specific changes located at the level of the slice.CC BY · PubMed Central
Figure 4 Differences between AD and control subjects for specific overlapping indices. (a) Gross tissue loss is indicated by areas where FA decreases overlap with MD increases. (b) Myelin damage is indicated by areas where FA decreases overlap with DR increases. (c) Microstructural damage in the absence of gross tissue loss is assessed by areas where FA decreases but MD remains unchanged. The left panels show three-dimensional models of the left hemisphere. The middle panels show three-dimensional models of the right hemisphere. The right panels show areas of changes restricted to a single sagittal slice to highlight the situation for the corpus callosum. See text for further details regarding overlapping indices.
Figure 4 Differences between AD and control subjects for specific overlapping indices. (a) Gross tissue loss is indicated by areas where FA decreases overlap with MD increases. (b) Myelin damage is indicated by areas where FA decreases overlap with DR increases. (c) Microstructural damage in the absence of gross tissue loss is assessed by areas where FA decreases but MD remains unchanged. The left panels show three-dimensional models of the left hemisphere. The middle panels show three-dimensional models of the right hemisphere. The right panels show areas of changes restricted to a single sagittal slice to highlight the situation for the corpus callosum. See text for further details regarding overlapping indices.CC BY · PubMed Central
Figure 5 Analysis of correlation between diffusion indices. (a) Correlation between FA and DR within a mask of the regions implicated in Figure 4 (b) where FA was significantly lower and DR was significantly higher in AD subjects relative to controls. (b) Correlation between FA and MD within a mask of the regions implicated in Figure 4 (a) where FA was significantly lower and MD was significantly higher in AD subjects relative to controls. The r value denotes the correlation as calculated by Pearson's product-moment correlation using data from all subjects. Correlations are significant as indicated by the p values.
Figure 5 Analysis of correlation between diffusion indices. (a) Correlation between FA and DR within a mask of the regions implicated in Figure 4 (b) where FA was significantly lower and DR was significantly higher in AD subjects relative to controls. (b) Correlation between FA and MD within a mask of the regions implicated in Figure 4 (a) where FA was significantly lower and MD was significantly higher in AD subjects relative to controls. The r value denotes the correlation as calculated by Pearson's product-moment correlation using data from all subjects. Correlations are significant as indicated by the p values.CC BY · PubMed Central
Figure 6 Analysis of disease progression with MCIna versus AD, and, MCIa versus AD. MCIna versus AD is shown in red, MCIa versus AD is shown in green, and areas where these contrasts overlap is shown in blue. (a) FA decreases together with DR increases. (b) FA decreases together with MD increases. (c) FA decreases where MD remains unchanged. See text main text for anatomical description and explanation of the three combinations of indices.
Figure 6 Analysis of disease progression with MCIna versus AD, and, MCIa versus AD. MCIna versus AD is shown in red, MCIa versus AD is shown in green, and areas where these contrasts overlap is shown in blue. (a) FA decreases together with DR increases. (b) FA decreases together with MD increases. (c) FA decreases where MD remains unchanged. See text main text for anatomical description and explanation of the three combinations of indices.CC BY · PubMed Central

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Research works printed but not linked: 1

  1. AZ Burzynska, 2010, Age-related differences in white matter microstructure: region-specific patterns of diffusivity., Neuroimage, 49, 2104, 10.1016/j.neuroimage.2009.09.041 · DOI

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Metadata

Authors
O'Dwyer, L., Lamberton, F., Bokde, A. L. W., Ewers, M., Faluyi, Y. O., Tanner, C., Mazoyer, B., O'Neill, D., Bartley, M., Collins, D. R., Coughlan, T., Prvulovic, D., & Hampel, H.
Affiliations
  • Centre National de la Recherche Scientifique (FR)
  • Trinity College Dublin (IE)
  • San Francisco VA Medical Center (US)
  • Cambridgeshire and Peterborough NHS Foundation Trust (GB)
  • Goethe University Frankfurt (DE)
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2011-06-30
Volume
6
Issue
6
Pages
e21745
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0021745
PMC
PMC3128090
OpenAlex
W2111813385
Cited by
119
References
86
Citations by year
2026: 1 · 2025: 5 · 2024: 2 · 2023: 9 · 2022: 5 · 2021: 6 · 2020: 7 · 2019: 7 · 2018: 4 · 2017: 10 · 2016: 8 · 2015: 10 · 2014: 10 · 2013: 19 · 2012: 14
FWCI
10.77
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Arrow@dit (Dublin Institute of Technology) (submittedVersion, cc-by-nc-sa)
  • HAL (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Publication Server of Goethe University Frankfurt am Main (Goethe University Frankfurt) (submittedVersion, cc-by)
Funders
  • Irish Research Council for Science, Engineering and Technology
  • Science Foundation Ireland (08/IN.1/B1846)
  • Irish Research Council
Topics
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
  • Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
Keywords
white matter injury, mild cognitive impairment, Alzheimer's disease, diffusion MRI, axial diffusion, radial diffusion, fractional anisotropy, tract-based spatial statistics, posterior cingulum, precuneus, prefrontal cortex, uncinate fasciculus, forceps minor, fornix, corpus callosum, temporal lobe, memory networks, disease progression
MeSH terms
Aged, Alzheimer Disease, Female, Humans, Male, Middle Aged, Diffusion Magnetic Resonance Imaging, Cognitive Dysfunction

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