Microstructural integrity of the cingulum is related to verbal memory performance in elderly with cerebral small vessel disease
Open accessAbstract
Background Cerebral small vessel disease (SVD) is related to verbal memory failures. It is suggested that early white matter damage, is located, among others, in the (posterior) cingulum at an early stage in neurodegeneration. Changes in the microstructural integrity of the cingulum assessed with diffusion tensor imaging (DTI), beyond detection with conventional MRI, may precede macrostructural changes and be related to verbal memory failures. Objective To investigate the relation between cingular microstructural integrity and verbal memory performance in 503 non-demented elderly with cerebral SVD. Methods The RUN DMC study is a prospective cohort study in elderly (50-85 years) with cerebral SVD. All participants underwent T1 MPRAGE, FLAIR and DTI scanning and the Rey Auditory Verbal Learning Test. Mean diffusivity (MD) and fractional anisotropy (FA) were assessed in six different cingular regions of interests (ROIs). Linear regression analysis was used to assess the relation between verbal memory performance and cingular DTI parameters, with appropriate adjustments. Furthermore a TBSS analysis of the whole brain was performed to investigate the specificity of our findings. Results Both our ROI-based and TBSS analysis showed that FA was positively related to immediate memory, delayed recall, delayed recognition and overall verbal memory performance of the cingulum, independent of confounders. A similar distribution was seen for the inverse association with MD and verbal memory performance with TBSS analysis. No significant relations were found with psychomotor speed, visuospatial memory and MMSE. When stratified on hippocampal integrity, the MD and FA values of the cingular ROIs differed significantly between participants with a good and poor hippocampal integrity. Conclusion Microstructural integrity of the cingulum, assessed by DTI, is specifically related to verbal memory performance, in elderly with SVD. Furthermore we found that when the integrity of the hippocampus is disrupted, the cingulum integrity is impaired as well.
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Correlations between cingulum microstructure and memory are more often described within clinical groups, e.g., in cerebral small vessel disease, mild traumatic injury, Mild Cognitive Impairment, and Alzheimer's disease.
“In contrast to the evidence from healthy populations, correlations between cingulum microstructure and memory are more often described within clinical groups, e.g., in cerebral small vessel disease (van der Holst et al., 2013), mild traumatic injury (Wu et al., 2010), Mild Cognitive Impairment (e.g., Metzler-Baddeley et al., 2012a, b, for meta-analysis see Yu et al., 2017) and Alzheimer’s disease”
From The cingulum bundle: Anatomy, function, and dysfunction (2018) · cites this paper as van der Holst et al., 2013
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Axon degeneration mechanisms: Commonality amid diversity
Coleman, M. (2005) · Nature reviews. Neuroscience · doi:10.1038/nrn1788 · Cited by 819 · see citing works
White matter damage on diffusion tensor imaging correlates with age-related cognitive decline
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- van Norden, A.G.W., de Laat, K.F., Gons, R.A., van Uden, I.W., van Dijk, E.J., van Oudheusden, L.J., Esselink, R.A., Bloem, B.R., van Engelen, B.G., Zwarts, M.J., Tendolkar, I., Olde-Rikkert, M.G., van der Vlugt, M.J., Zwiers, M.P., Norris, D.G., de Leeuw, F.E., 2011a. Causes and consequences of cerebral small vessel disease. The RUN DMC study: a prospective cohort study. Study rationale and protocol. BMC Neurol. http://dx.doi.org/10.1186/1471-2377-11-29(Epub). · DOI
- van Norden, A.G.W., de Laat, K.F., Fick, I., van Uden, I.W.M., van Oudheusden, L.J.B., Gons, R.A.R., Norris, D.G., Zwiers, M.P., Kessels, R.P.C., de Leeuw, F.E., 2011b. Diffu- sion tensor imaging of the hippocampus and verbal memory performance: the RUN DMC Study. Hum. Brain Mapp. http://dx.doi.org/10.1002/hbm.21231(Epub). · DOI
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The cingulum bundle: Anatomy, function, and dysfunction
Bubb, E. J., Metzler-Baddeley, C., & Aggleton, J. P. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.05.008 · Cited by 740 · see citing works
White matter integrity in small vessel disease is related to cognition
Tuladhar, A. M., van Norden, A. G. W., de Laat, K. F., Zwiers, M. P., van Dijk, E. J., Norris, D. G., & de Leeuw, F.-E. (2015) · NeuroImage: Clinical · doi:10.1016/j.nicl.2015.02.003 · Cited by 182 · see citing works
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- Authors
- van der Holst, H. M., Tuladhar, A. M., van Norden, A. G. W., de Laat, K. F., van Uden, I. W. M., van Oudheusden, L. J. B., Zwiers, M. P., Norris, D. G., Kessels, R. P. C., & de Leeuw, F. E.
- Affiliations
- Radboud University Nijmegen (NL)
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2013-01
- Volume
- 65
- Pages
- 416-423
- ISSN
- 1053-8119 (ISSN-L)
- OpenAlex
- W2143948729
- Cited by
- 38
- References
- 3
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 1 · 2023: 3 · 2022: 5 · 2021: 2 · 2020: 2 · 2019: 4 · 2018: 2 · 2017: 2 · 2016: 3 · 2015: 6 · 2014: 4
- FWCI
- 2.09
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- Universitätsbibliographie, Universität Duisburg-Essen (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Pure Amsterdam UMC (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Dutch Brain Foundation (H04-12)
- Netherlands Organization Scientific Research (40-00703-97-07197)
- Internationale Stichting Alzheimer Onderzoek
- VIDI innovational grant (452-08-005)
- Topics
- Health Sciences › Medicine › Neurology › Cerebrovascular and genetic disorders
- 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
- Keywords
- cerebral small vessel disease, cingulum, verbal memory, white matter microstructure, fractional anisotropy, mean diffusivity, hippocampal integrity, older adults, neurodegeneration, diffusion tensor imaging, Rey Auditory Verbal Learning Test
- MeSH terms
- Aged, Aged, 80 and over, Female, Gyrus Cinguli, Humans, Image Interpretation, Computer-Assisted, Male, Memory, Memory Disorders, Middle Aged, Neuropsychological Tests, Cohort Studies, Diffusion Magnetic Resonance Imaging, Cerebral Small Vessel Diseases
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