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Cited by 132Functional Brain Connectivity StudiesDementia and Cognitive Impairment ResearchAlzheimer's disease research and treatments

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Single-Subject Grey Matter Graphs in Alzheimer's Disease

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Tijms, Betty M., Möller, Christiane, Vrenken, Hugo, Wink, Alle Meije, de Haan, Willem, van der Flier, Wiesje M., Stam, Cornelis J., Scheltens, Philip, Barkhof, Frederik·2013·PLoS ONE
DOI 10.1371/journal.pone.0058921PMC PMC3594199
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Abstract

Coordinated patterns of cortical morphology have been described as structural graphs and previous research has demonstrated that properties of such graphs are altered in Alzheimer's disease (AD). However, it remains unknown how these alterations are related to cognitive deficits in individuals, as such graphs are restricted to group-level analysis. In the present study we investigated this question in single-subject grey matter networks. This new method extracts large-scale structural graphs where nodes represent small cortical regions that are connected by edges when they show statistical similarity. Using this method, unweighted and undirected networks were extracted from T1 weighted structural magnetic resonance imaging scans of 38 AD patients (19 female, average age 72±4 years) and 38 controls (19 females, average age 72±4 years). Group comparisons of standard graph properties were performed after correcting for grey matter volumetric measurements and were correlated to scores of general cognitive functioning. AD networks were characterised by a more random topology as indicated by a decreased small world coefficient (p = 3.53×10(-5)), decreased normalized clustering coefficient (p = 7.25×10(-6)) and decreased normalized path length (p = 1.91×10(-7)). Reduced normalized path length explained significantly (p = 0.004) more variance in measurements of general cognitive decline (32%) in comparison to volumetric measurements (9%). Altered path length of the parahippocampal gyrus, hippocampus, fusiform gyrus and precuneus showed the strongest relationship with cognitive decline. The present results suggest that single-subject grey matter graphs provide a concise quantification of cortical structure that has clinical value, which might be of particular importance for disease prognosis. These findings contribute to a better understanding of structural alterations and cognitive dysfunction in AD.

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Figure 1 Box plots visualising differences in the distributions of global graph property values between Alzheimer's disease patients (AD) and control subjects (C). Box plots show the distributions of: a) grey matter volume: F (1, 74) = 13.78, p = 0.0004, b) the average path length: F (1, 71) = 19.62, p = 3.35×10−5, c) the average clustering coefficient: F (1, 71) = 4.58, p = 0.04, d) average λ: F(1, 71) = 33.30, p = 1.91×10−7, e) average γ: F (1, 71) = 23.45, p = 7.25×10−6 and f) the small world property F (1, 71) = 19.50, p = 3.53×10−5. Middle line indicates the median value, the cross indicates the mean. * = p<0.05; *** = p<0.001, significance of ANCOVAs after adjustment of total volume, age and gender.
Figure 1 Box plots visualising differences in the distributions of global graph property values between Alzheimer's disease patients (AD) and control subjects (C). Box plots show the distributions of: a) grey matter volume: F (1, 74) = 13.78, p = 0.0004, b) the average path length: F (1, 71) = 19.62, p = 3.35×10−5, c) the average clustering coefficient: F (1, 71) = 4.58, p = 0.04, d) average λ: F(1, 71) = 33.30, p = 1.91×10−7, e) average γ: F (1, 71) = 23.45, p = 7.25×10−6 and f) the small world property F (1, 71) = 19.50, p = 3.53×10−5. Middle line indicates the median value, the cross indicates the mean. * = p<0.05; *** = p<0.001, significance of ANCOVAs after adjustment of total volume, age and gender.CC BY · PubMed Central
Figure 2 The spatial distribution of betweenness centrality (BC) values across the cortex, group differences in local BC and local path length. a) BC values were averaged over subjects in the Alzheimer's disease (AD, upper panel) and control (C, lower panel) groups. After individual maps were normalised for graph size they were warped into MNI space where they were averaged for each group. Average maps were normalised again to values between 0–1. The spatial distribution of the unnormalised BC values showed a strong correlation between the groups (ρ = 0.74, p<2.2×10−16). b) Surface plots of the F values of the AAL regions that showed a significantly decreased average BC value after correction for local grey matter volume, gender and age. c) Surface plots of the 20 AAL regions that showed a significant (p<0.05) correlation between local path length (L) and mini-mental state examination (MMSE) scores (See Figure S1 in File S1 for the scatter plots of all significant correlations).
Figure 2 The spatial distribution of betweenness centrality (BC) values across the cortex, group differences in local BC and local path length. a) BC values were averaged over subjects in the Alzheimer's disease (AD, upper panel) and control (C, lower panel) groups. After individual maps were normalised for graph size they were warped into MNI space where they were averaged for each group. Average maps were normalised again to values between 0–1. The spatial distribution of the unnormalised BC values showed a strong correlation between the groups (ρ = 0.74, p<2.2×10−16). b) Surface plots of the F values of the AAL regions that showed a significantly decreased average BC value after correction for local grey matter volume, gender and age. c) Surface plots of the 20 AAL regions that showed a significant (p<0.05) correlation between local path length (L) and mini-mental state examination (MMSE) scores (See Figure S1 in File S1 for the scatter plots of all significant correlations).CC BY · PubMed Central
Figure 3 Scatter plots of rank-transformed scores on the mini-mental state examination (MMSE) with global path length L and λ. Correlations between MMSE and L (a) and λ (norm. L.; b) for the AD (black circles) and control group (dark grey plus signs). Note that global grey matter volume, graph size and connectivity density were unrelated to MMSE scores (resp. r = −0.18, p = 0.28; r = −0.18, p = 0.29; r = −0.06, p = 0.73), nor were such relationships found with local grey matter in any of the AAL regions.
Figure 3 Scatter plots of rank-transformed scores on the mini-mental state examination (MMSE) with global path length L and λ. Correlations between MMSE and L (a) and λ (norm. L.; b) for the AD (black circles) and control group (dark grey plus signs). Note that global grey matter volume, graph size and connectivity density were unrelated to MMSE scores (resp. r = −0.18, p = 0.28; r = −0.18, p = 0.29; r = −0.06, p = 0.73), nor were such relationships found with local grey matter in any of the AAL regions.CC BY · PubMed Central

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Metadata

Authors
Tijms, B. M., Möller, C., Vrenken, H., Wink, A. M., de Haan, W., van der Flier, W. M., Stam, C. J., Scheltens, P., & Barkhof, F.
Affiliations
Amsterdam UMC Location Vrije Universiteit Amsterdam (NL)
Corresponding author
Tijms, Betty M.
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2013-03-11
Volume
8
Issue
3
Pages
e58921
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0058921
PMC
PMC3594199
OpenAlex
W2058087702
Cited by
132
References
102
Citations by year
2026: 2 · 2025: 6 · 2024: 12 · 2023: 8 · 2022: 11 · 2021: 15 · 2020: 11 · 2019: 6 · 2018: 18 · 2017: 11 · 2016: 10 · 2015: 12 · 2014: 7 · 2013: 3
FWCI
5.85
Type
journal article
Language
en
Update notices
correction (2013-09-09)
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • UCL Discovery (University College London) (submittedVersion)
  • Pure Amsterdam UMC (submittedVersion)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
  • Data Archiving and Networked Services (DANS) (submittedVersion)
Funders
  • Stichting Dioraphte
  • Alzheimer Nederland
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
  • 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
Alzheimer's disease, structural graph, small-world property, path length, clustering coefficient, cognitive decline, cortical morphology, hippocampus, parahippocampal gyrus, precuneus, fusiform gyrus, gray matter volume, disease prognosis
MeSH terms
Aged, Alzheimer Disease, Brain Mapping, Electroencephalography, Female, Humans, Magnetic Resonance Imaging, Male, Psychiatric Status Rating Scales, Severity of Illness Index, Case-Control Studies, Neuroimaging

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