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Cited by 79Advanced Neuroimaging Techniques and ApplicationsDementia and Cognitive Impairment ResearchCerebrovascular and genetic disorders

Diffusion models reveal white matter microstructural changes with ageing, pathology and cognition

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Raghavan, Sheelakumari, Reid, Robert I, Przybelski, Scott A, Lesnick, Timothy G, Graff-Radford, Jonathan, Schwarz, Christopher G, Knopman, David S, Mielke, Michelle M +4 more·2021·Brain Communications
DOI 10.1093/braincomms/fcab106PMC PMC8202149
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Abstract

White matter microstructure undergoes progressive changes during the lifespan, but the neurobiological underpinnings related to ageing and disease remains unclear. We used an advanced diffusion MRI, Neurite Orientation Dispersion and Density Imaging, to investigate the microstructural alterations due to demographics, common age-related pathological processes (amyloid, tau and white matter hyperintensities) and cognition. We also compared Neurite Orientation Dispersion and Density Imaging findings to the older Diffusion Tensor Imaging model-based findings. Three hundred and twenty-eight participants (264 cognitively unimpaired, 57 mild cognitive impairment and 7 dementia with a mean age of 68.3 ± 13.1 years) from the Mayo Clinic Study of Aging with multi-shell diffusion imaging, fluid attenuated inversion recovery MRI as well as amyloid and tau PET scans were included in this study. White matter tract level diffusion measures were calculated from Diffusion Tensor Imaging and Neurite Orientation Dispersion and Density Imaging. Pearson correlation and multiple linear regression analyses were performed with diffusion measures as the outcome and age, sex, education/occupation, white matter hyperintensities, amyloid and tau as predictors. Analyses were also performed with each diffusion MRI measure as a predictor of cognitive outcomes. Age and white matter hyperintensities were the strongest predictors of all white matter diffusion measures with low associations with amyloid and tau. However, neurite density decrease from Neurite Orientation Dispersion and Density Imaging was observed with amyloidosis specifically in the temporal lobes. White matter integrity (mean diffusivity and free water) in the corpus callosum showed the greatest associations with cognitive measures. All diffusion measures provided information about white matter ageing and white matter changes due to age-related pathological processes and were associated with cognition. Neurite orientation dispersion and density imaging and diffusion tensor imaging are two different diffusion models that provide distinct information about variation in white matter microstructural integrity. Neurite Orientation Dispersion and Density Imaging provides additional information about synaptic density, organization and free water content which may aid in providing mechanistic insights into disease progression.

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  • NODDI provides enhanced sensitivity and specific metrics for detecting Alzheimer's disease-associated microstructural changes.

    “In contrast, NODDI provides enhanced sensitivity and specific metrics for detecting AD‐associated microstructural changes. 31 , 32 , 33”

    From Apolipoprotein ε4 exacerbates white matter impairment in a mouse model of Aβ amyloidosis by decreasing actively myelinating oligodendrocytes (2025) · cites this paper as [31]

    The Discussion (page not provided) reports that NODDI metrics detected Alzheimer’s disease–related white-matter changes and offered more detailed information about neurite health. It does not establish enhanced detection sensitivity over DTI: the Introduction frames that as a hypothesis, and the Discussion says both methods detected subtle Alzheimer’s disease–related changes. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Multi-shell approaches, including NODDI, constrained NODDI (C-NODDI), and diffusion kurtosis imaging, provide model-dependent indices related to neurite organization, extracellular water, axonal density, and tissue integrity.

    “Multi-shell approaches, including NODDI, constrained NODDI (C-NODDI), and diffusion kurtosis imaging, provide model-dependent indices related to neurite organization, extracellular water, axonal density, and tissue integrity (Alsameen et al., 2023; Raghavan et al., 2021; Schilling et al., 2022).”

    From 40 Years of diffusion MRI in the brain: From history to emerging frontiers (2026) · cites this paper as Raghavan et al., 2021

    The Introduction describes multi-shell NODDI and its indices for neurite density, orientation dispersion, and free-water fraction; the Discussion relates these measures to white matter microstructure. The passages support the NODDI portion, but do not address constrained NODDI (C-NODDI) or diffusion kurtosis imaging. (LLM, conf=0.86)

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Authors
Raghavan, S., Reid, R. I., Przybelski, S. A., Lesnick, T. G., Graff-Radford, J., Schwarz, C. G., Knopman, D. S., Mielke, M. M., Machulda, M. M., Petersen, R. C., Jack, C. R., & Vemuri, P.
Affiliations
  • Mayo Clinic (US)
  • Department of Neurology, Mayo Clinic, Rochester, MN 55905, USA
Corresponding author
Vemuri, Prashanthi
ORCID
Venue
Brain Communications
Publisher
Oxford University Press (OUP)
Published
2021-04-01
Volume
3
Issue
2
Pages
fcab106-fcab106
ISSN
2632-1297 (ISSN-L)
DOI
10.1093/braincomms/fcab106
PMC
PMC8202149
OpenAlex
W3160467514
Cited by
79
References
10
Citations by year
2026: 10 · 2025: 25 · 2024: 15 · 2023: 17 · 2022: 10 · 2021: 2
FWCI
5.81
Type
journal article
Language
en
Open access
Licence
Locations
  • Brain Communications (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • National Institute of Health (R01 NS097495, R01 AG56366, U01 AG06786, P50 AG16574, R37 AG11378, R01 AG41851)
  • Gerald and Henrietta Rauenhorst Foundation
  • Alzheimer’s Drug Discovery Foundation
  • Alexander Family Alzheimer’s Disease Research Professorship of the Mayo Foundation
  • Liston Award, Elsie and Marvin Dekelboum Family Foundation
  • Schuler Foundation
  • Opus building National Institute of Health (C06 RR018898)
  • Rochester Epidemiology Project (R01 AG34676)
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
  • Health Sciences › Medicine › Neurology › Cerebrovascular and genetic disorders
Keywords
white matter microstructure, aging, NODDI, diffusion tensor imaging, white matter hyperintensities, amyloid, tau protein, mild cognitive impairment, dementia, corpus callosum, mean diffusivity, free water, synaptic density, temporal lobe, Mayo Clinic Study of Aging

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