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DTI measures in crossing-fibre areas: increased diffusion anisotropy reveals early white matter alteration in MCI and mild Alzheimer’s disease
Open accessAbstract
Though mild cognitive impairment is an intermediate clinical state between healthy aging and Alzheimer's disease (AD), there are very few whole-brain voxel-wise diffusion MRI studies directly comparing changes in healthy control, mild cognitive impairment (MCI) and AD subjects. Here we report whole-brain findings from a comprehensive study of diffusion tensor indices and probabilistic tractography obtained in a very large population of healthy controls, MCI and probable AD subjects. As expected from the literature, all diffusion indices converged to show that the cingulum bundle, the uncinate fasciculus, the entire corpus callosum and the superior longitudinal fasciculus are the most affected white matter tracts in AD. Significant differences between MCI and AD were essentially confined to the corpus callosum. More importantly, we introduce for the first time in a degenerative disorder an application of a recently developed tensor index, the "mode" of anisotropy, as well as probabilistic crossing-fibre tractography. The mode of anisotropy specifies the type of anisotropy as a continuous measure reflecting differences in shape of the diffusion tensor ranging from planar (e.g., in regions of crossing fibres from two fibre populations of similar density or regions of "kissing" fibres) to linear (e.g., in regions where one fibre population orientation predominates), while probabilistic crossing-fibre tractography allows to accurately trace pathways from a crossing-fibre region. Remarkably, when looking for whole-brain diffusion differences between MCI patients and healthy subjects, the only region with significant abnormalities was a region of crossing fibres in the centrum semiovale, showing an increased mode of anisotropy. The only white matter region demonstrating a significant difference in correlations between neuropsychological scores and a diffusion measure (mode of anisotropy) across the three groups was the same region of crossing fibres. Further examination using probabilistic tractography established explicitly and quantitatively that this previously unreported increase of mode and co-localised increase of fractional anisotropy was explained by a relative preservation of motor-related projection fibres (at this early stage of the disease) crossing the association fibres of the superior longitudinal fasciculus. These findings emphasise the benefit of looking at the more complex regions in which spared and affected pathways are crossing to detect very early alterations of the white matter that could not be detected in regions consisting of one fibre population only. Finally, the methods used in this study may have general applicability for other degenerative disorders and, beyond the clinical sphere, they could contribute to a better quantification and understanding of subtle effects generated by normal processes such as visuospatial attention or motor learning.
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“In particular, major fibre tracts such as the forceps major and forceps minor, inferior fronto-occipital fasciculus as well as the posterior cingulum show white matter alterations in Alzheimer’s disease dementia (Taylor et al., 2001; Teipel et al., 2002; Douaud et al., 2011; Mito et al., 2018).”
From White matter diffusion alterations precede symptom onset in autosomal dominant Alzheimer’s disease (2018) · cites this paper as Douaud et al., 2011
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“DTI alterations such as those observed in the corticospinal tract in the current study should be interpreted with caution, as the current TBSS approach cannot be unambiguously attributed to that tract, but potentially are because of alterations in crossing fibres such as the superior longitudinal fasciculus or corpus callosum (Douaud et al., 2011; Teipel et al., 2014; Mito et al., 2018).”
From White matter diffusion alterations precede symptom onset in autosomal dominant Alzheimer’s disease (2018) · cites this paper as Douaud et al., 2011
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“In healthy tissue with crossing fibers, the DTI model may show low FA. FADTI may paradoxically appear to increase in regions where crossing fibers deteriorate in neurodegenerative diseases such as AD (Douaud et al., 2011).”
From Diffusion MRI Indices and Their Relation to Cognitive Impairment in Brain Aging: The Updated Multi-protocol Approach in ADNI3 (2019) · cites this paper as Douaud et al., 2011
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“However, very little is known about the effects of crossing fibers on estimated cross-subject differences in conventional DTI measures [20].”
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“…white matter integrity or loss of axons (Jones, Knösche, & Turner, 2013) and increases in FA have been shown in the brains of individuals with neurodegenerative disease (e.g. Douaud et al., 2011), which might explain the accelerated decrease in left prefrontal FA relative to right prefrontal FA.”
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“However, higher FA has also been associated with poorer behavioral outcomes (Tuch et al., 2005; Hoeft et al., 2007) and neuropathology (Douaud et al., 2011).”
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“Selectively lowered μFA in one out of many crossing fiber populations may even lead to an increased FA at a voxel level.(42) Dispersion is a particularly acute problem in more heterogeneous tissues, most notably in cortical gray matter, where the macroscopic FA is negligible, but μFA, in contrast, can retrieve informa…”
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“However, where nerves cross, an atypical increase in FA may occur owing to a higher apparent diffusion coefficient of the other nerve when one nerve is damaged (75).”
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“The importance of this was demonstrated in an earlier imaging-study comparing changes in DTI-derived summary measures in areas of crossing fibres pertaining to data from Alzheimer disease (AD), MCI, and healthy aging subjects [93].”
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“For example, a loss of axons could result in decreased fractional anisotropy; however, in the presence of unaffected crossing fibre structures, loss of axons could result in increased anisotropy in that region 25,27 .”
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“For example, in Alzheimer’s disease, increased FA may reflect pathological changes in fiber orientation dispersion 30.31 .”
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“At the same time no significant differences in the mode of anisotropy, a measure sensitive to changes in fibre orientation predominance (Douaud et al., 2011), were seen.”
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“Decreases in the AD are possibly due to increased debris from membrane disruption during axonal degeneration [35] or complex changes in fiber architecture [36].”
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Investigating Tissue-Specific Abnormalities in Alzheimer’s Disease with Multi-Shell Diffusion MRI
Giraldo, D. L., Smith, R. E., Struyfs, H., Niemantsverdriet, E., Roeck, E. E. D., Bjerke, M., Engelborghs, S., Romero, E., Sijbers, J., & Jeurissen, B. (2022) · Journal of Alzheimer s Disease · doi:10.3233/jad-220551 · Cited by 10
“In the corticospinal pathway, previous works have reported reduced mean kurtosis, increased free-water index, and increased FA in regions where the corticospinal tracts cross with other ones [20, 28, 32, 36, 43], which can be observed when WM degeneration occurs in a subset of crossing fiber populations.”
BackgroundOne-year changes in brain microstructure differentiate preclinical Huntington's disease stages
Pflanz, C. P., Charquero‐Ballester, M., Majid, D. S. A., Winkler, A. M., Vallée, E., Aron, A. R., Jenkinson, M., & Douaud, G. (2019) · NeuroImage Clinical · doi:10.1016/j.nicl.2019.102099 · Cited by 9
“We used the FMRIB software library (FSL, version 5.0.4) (Smith et al., 2004; Jenkinson et al., 2012) to pre-process the MRI data.”
InfluentialAnalytical performance bounds for multi-tensor diffusion-MRI
Sid, F. A., Abed‐Meraim, K., Harba, R., & Oulebsir-Boumghar, F. (2016) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2016.10.014 · Cited by 9
Tato-Fernández, C., Ekblad, L. L., Pietilä, E. M., Saunavaara, V., Helin, S., Parkkola, R. K., Zetterberg, H., Blennow, K., Rinne, J. O., & Snellman, A. (2024) · Neurobiology of Disease · doi:10.1016/j.nbd.2024.106439 · Cited by 9
“…DTI studies report degeneration of white matter tracts in healthy APOE4 carriers (Bage-pally et al., 2012; Cai et al., 2017; Cavedo et al., 2017; Douaud et al., 2011; Dowell et al., 2013; Gold et al., 2010; Heise et al., 2014; Nier-enberg et al., 2005; Persson et al., 2006), but other…”
BackgroundDiscriminating VCID subgroups: A diffusion MRI multi-model fusion approach
Raja, R., Caprihan, A., Rosenberg, G., Rachakonda, S., & Calhoun, V. (2020) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2020.108598 · Cited by 6
“These measures showed differences in both whole brain tractograms and specific WM tracts between AD and controls [42–44].”
BackgroundResultKeong, N. C. H., Lock, C., Soon, S., Hernowo, A. T., Czosnyka, Z. H., Czosnyka, M., Pickard, J. D., & Narayanan, V. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2022.868026 · Cited by 8
Diffusion MRI in Neurological Disorders
Bodini, B., & Ciccarelli, O. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-396460-1.00011-1 · Cited by 8
Structural Connectivity Affecting Aspiration After Stroke
Yang, H.-E., Kang, H., Kyeong, S., & Kim, D. H. (2021) · Dysphagia · doi:10.1007/s00455-021-10388-z · Cited by 8
“Hence, increased FA and MO values are considered to indicate degeneration of one fiber among crossing fibers in brain regions, present mainly in the internal capsule of the right hemisphere in this study [8, 10].”
BackgroundAli, T., Lv, J., & Calamante, F. (2022) · Magnetic Resonance in Medicine · doi:10.1002/mrm.29413 · Cited by 8
Dávid, S., Mesri, H. Y., Bodiut, V. A., Nagtegaal, S., Elhalawani, H. M., Luca, A. D., Philippens, M. E. P., Viergever, M. A., Mohamed, A., Ding, Y., et al. (2019) · medRxiv · doi:10.1101/19005157 · Cited by 8
“The exact underlying mechanisms are ambiguous, since changes of FA are not specific to one well-defined procedure, like demyelination, scarification [60] and axonal loss [61].”
BackgroundMasdeu, J. C. (2016) · Handbook of clinical neurology · doi:10.1016/b978-0-444-53486-6.00048-x · Cited by 7
Lee, S., Pyun, S., & Tae, W. (2019) · Neuroradiology · doi:10.1007/s00234-019-02178-0 · Cited by 7
Tinney, E. M., Loui, P., Raine, L. B., Hiscox, L. V., Delgorio, P. L., Kramer, M. K., Schwarb, H. D., Martens, C. R., Kramer, A. F., Hillman, C. H., et al. (2023) · Psychophysiology · doi:10.1111/psyp.14306 · Cited by 8
“Based on previous evidence, the most prominent group differences were expected in the corpus callosum (Douaud et al., 2011), the superior longitudinal fasciculus (Douaud et al., 2011), the forceps minor (Bartzokis, 2011), and the retrolenticular part of the internal capsule (Shim et al., 2017).”
MethodKaran, P., Reymbaut, A., Gilbert, G., & Descoteaux, M. (2021) · Medical Image Analysis · doi:10.1016/j.media.2022.102476 · Cited by 7
Tu, M.-C., Huang, S., Hsu, Y., Yang, J., Lin, C.-Y. E., & Kuo, L. (2024) · Scientific Reports · doi:10.1038/s41598-024-52910-x · Cited by 7
“As the DKI metrics were derived from a WMA driven by FA, the possibility of pseudo-normalization of KFA values when the quantification process involves crossing fibers as documented issues in FA calculations should be considered 17 .”
MethodSchmidt, M. A., Mennecke, A., Michelson, G., Doerfler, A., & Engelhorn, T. (2014) · PLoS ONE · doi:10.1371/journal.pone.0099344 · Cited by 7
“This approach has been used before in TBSS analysis of patients with Alzheimer’s disease who had ventricular enlargement due to atrophy [14].”
MethodMamiya, P. C., Richards, T. L., Corrigan, N. M., & Kuhl, P. K. (2020) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.02869 · Cited by 7
(2013) · Elsevier eBooks · doi:10.1016/b978-0-12-398398-5.00008-4 · Cited by 7
Estimation of diffusion properties in three-way fiber crossings without overfitting
Yang, J., Poot, D. H. J., A, L. J. V. V., & Vos, F. M. (2015) · Physics in Medicine and Biology · doi:10.1088/0031-9155/60/23/9123 · Cited by 6
Genetic and degenerative disorders primarily causing dementia
Masdeu, J. C., & Pascual, B. (2016) · Handbook of clinical neurology · doi:10.1016/b978-0-444-53485-9.00026-x · Cited by 6
“However, higher anisotropy can be found in white-matter volumes where a disrupted tract, such as the superior longitudinal fasciculus, crosses an intact one, such as the corticospinal tract, effectively increasing volume anisotropy (Douaud et al., 2011).”
Ramírez‐Toraño, F., Abbas, K., Bruña, R., Pedro, S. M.-D., Gómez‐Ruiz, N., Barabash, A., Pereda, E., Marcos, A., López-Higes, R., Maestú, F., et al. (2021) · Cerebral Cortex Communications · doi:10.1093/texcom/tgab051 · Cited by 7
“…impairment (MCI) is a decreased in fractional anisotropy (FA) and an increase in mean diffusivity (MDiff), especially in the hippocampal cingulum and in the posterior, temporal and parietal areas white matter (WM) (Bozzali et al. 2002; Douaud et al. 2011; Nir et al. 2013; Mayo et al. 2019).”
BackgroundQuantification of Tissue Microstructure Using Tensor-Valued Diffusion Encoding: Brain and Body
Afzali, M., Mueller, L., Szczepankiewicz, F., Jones, D. K., & Schneider, J. E. (2022) · Frontiers in Physics · doi:10.3389/fphy.2022.809133 · Cited by 7
“In the presence of crossing fibers, the degeneration in one set of fibers may cause an increase in the FA value [126] while the anisotropy is decreased microscopically.”
BackgroundLee, W., Park, B., & Han, K. (2015) · Lecture notes in computer science · doi:10.1007/978-3-319-22186-1_49 · Cited by 8
Age-related differences in white matter: Comparing fixel based and tensor based analysesPreprint
Kelley, S., Plass, J., Bender, A. R., & Polk, T. (2019) · bioRxiv · doi:10.1101/751628 · Cited by 7
Handiru, V. S., Alivar, A., Hoxha, A., Saleh, S., Suviseshamuthu, E. S., Yue, G. H., & Allexandre, D. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.08.332353 · Cited by 4
“Furthermore, reduced MA would signify more disc-like, less cigar-like shape water diffusion, i.e., more fiber crossing and less unidirectional fiber bundle (Douaud et al., 2011; Yoncheva et al., 2016), which could reflect the deterioration and thinning of WM tracts.”
BackgroundEvidence of Genetic Overlap Between Circadian Preference and Brain White Matter Microstructure
García‐Marín, L. M., Alcauter, S., Campos, A. I., Mulcahy, A., Kho, P. F., Cuéllar-Partida, G., & Rentería, M. E. (2021) · Twin Research and Human Genetics · doi:10.1017/thg.2021.4 · Cited by 5
“Although it is expected to observe crossing fibers in superior corona radiata and the retrolenticular portion of the internal capsule, such an increase in MO may be attributed to decreased quality (less densely packed fibers and axonal density) of a portion of the crossing fibers, resulting in a predominant fiber popu…”
ResultTomita, H., Kamagata, K., Andica, C., Uchida, W., Fukuo, M., Waki, H., Sugano, H., Tange, Y., Mitsuhashi, T., Lukies, M. W., et al. (2021) · Journal of Neuroscience Research · doi:10.1002/jnr.24912 · Cited by 4
“The inability to resolve multiple fiber orientations in regions of crossing or kissing fibers, which include up to 90% of the WM voxels in the brain, may contribute to an unreliable estimation of connectome mapping in these regions (Douaud et al., 2011).”
BackgroundNasser, N. S., Rajan, S., Venugopal, V. K., Lasič, S., Mahajan, V., & Mahajan, H. (2022) · Journal of Clinical Neuroscience · doi:10.1016/j.jocn.2022.05.027 · Cited by 6
Li, L., Yang, W., Wan, Y., Shen, H., Wang, T., Ping, L., Liu, C., Chen, M., Yu, H., Jin, S., et al. (2023) · Brain Imaging and Behavior · doi:10.1007/s11682-023-00791-5 · Cited by 5
“…et al., 2017; Haller et al., 2010, 2014; Teipel et al., 2010 ; Wang et al., 2012; Sun et al., 2014 ; Duffy et al., 2014 ; Bosch et al., 2012; Douaud et al., 2011; Zhuang et al., 2010; Setiadi et al., 2021; Zhang et al., 2019; Liu et al., 2013 ; O’Dwyer et al., 2011 ; Woodward et al., 2017;…”
InfluentialNeuroimaging Findings in Mild Cognitive Impairment
Nobili, F. M., Arnaldi, D., Roccatagliata, L., Chincarini, A., Accardo, J., Picco, A., Ferrara, M., Buschiazzo, A., & Morbelli, S. D. (2014) · Springer eBooks · doi:10.1007/978-3-642-54307-4_12 · Cited by 5
Crystallinity characterization of white matter in the human brain
Teich, E., Cieslak, M., Giesbrecht, B., Vettel, J., Grafton, S. T., Satterthwaite, T., & Bassett, D. (2020) · New Journal of Physics · doi:10.1088/1367-2630/ac1286 · Cited by 5
Brain Connectivity Affecting Gait Function after Unilateral Supratentorial Stroke
Lee, H. A., & Kim, D. (2021) · Brain Sciences · doi:10.3390/brainsci11070870 · Cited by 5
“Higher MO values show that one fiber predominates rather than indicating the presence of crossing fibers [10,16].”
BackgroundHe, F., Initiative, A. D. N., Zhang, Y., Wu, X., Li, Y., Zhao, J., Fang, P., Fan, L., Li, C., Liu, T., et al. (2021) · Journal of Alzheimer s Disease · doi:10.3233/jad-210495 · Cited by 5
Nishioka, C., Liang, H., Ong, S., & Sun, S. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.06.025 · Cited by 5
Autism detection based on multiple time scale model
Qin, C., Zhu, X., Ye, L., Li, P., Li, L., Wang, J., Ma, J., & Liu, T. (2022) · Journal of Neural Engineering · doi:10.1088/1741-2552/ac8b39 · Cited by 5
Haddad, S. M. H., Pieruccini‐Faria, F., Montero‐Odasso, M., & Bartha, R. (2023) · Journal of Alzheimer s Disease · doi:10.3233/jad-220476 · Cited by 7
Aganj, I., Mora, J., Frau‐Pascual, A., Fischl, B. R., & Initiative, A. D. N. (2023) · Alzheimer s & Dementia Diagnosis Assessment & Disease Monitoring · doi:10.1002/dad2.12511 · Cited by 4
Genetic variation in the G72 gene is associated with increased frontotemporal fiber tract integrity
Nickl‐Jockschat, T., Stöcker, T., Krug, A., Markov, V., Maximov, I. I., Huang, R., Schneider, F. W., Habel, U., Eickhoff, S. B., Zerres, K., et al. (2014) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-014-0516-6 · Cited by 5
“For each individual subject in the wild-type and the homozygous risk allele carrier group, the values of MO were averaged using as a mask results of our previous TBSS analysis of FA changes [58].”
MethodCorrelating Function and Imaging Measures of the Medial Longitudinal Fasciculus
Sakaie, K., Takahashi, M., Remington, G. M., Wang, X., Conger, A., Conger, D. L., Dimitrov, I. E., Jones, S., Frohman, A. N., Frohman, T. C., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0147863 · Cited by 5
“For example, low FA is typically interpreted as an indicator of tissue injury, but elevated FA has been associated with injury due to Alzheimer’s disease [21].”
BackgroundBergamino, M., Nelson, M. R., Numani, A., Scarpelli, M., Healey, D., Fuentes, A., Turner, G., & Stokes, A. M. (2023) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2023.03.024 · Cited by 4
Hierarchical modelling of crossing fibres in the white matter
Rafipoor, H., Lange, F. J., Arthofer, C., Cottaar, M., & Jbabdi, S. (2025) · Imaging Neuroscience · doi:10.1162/imag_a_00436 · Cited by 4
Progressive Myoclonus Epilepsy: Distinctive MRI Changes in Cerebellar and Motor Networks
Cameron, J., Mito, R., Berkovic, S., & Jackson, G. D. (2025) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.70010 · Cited by 4
Metadata
- Authors
- Douaud, G., Jbabdi, S., Behrens, T. E. J., Menke, R. A., Gass, A., Monsch, A. U., Rao, A., Whitcher, B., Kindlmann, G., Matthews, P. M., & Smith, S.
- Affiliations
- University of Oxford (GB)
- University Hospital of Basel (CH)
- GlaxoSmithKline (United Kingdom) (GB)
- University of Chicago (US)
- Corresponding author
- Douaud, Gwenaëlle
- ORCID
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2011-04
- Volume
- 55
- Issue
- 3
- Pages
- 880-890
- ISSN
- 1053-8119 (ISSN-L)
- PMC
- PMC7116583
- OpenAlex
- W2151712416
- Cited by
- 514
- References
- 66
- Citations by year
- 2026: 19 · 2025: 23 · 2024: 17 · 2023: 16 · 2022: 26 · 2021: 42 · 2020: 34 · 2019: 42 · 2018: 36 · 2017: 36 · 2016: 35 · 2015: 41 · 2014: 41 · 2013: 51 · 2012: 39
- FWCI
- 26.77
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- UK Engineering and Physical Sciences Research Council
- UK Medical Research Council
- Wellcome Trust
- 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
- mild cognitive impairment, Alzheimer's disease, white matter microstructure, crossing fibers, diffusion anisotropy, probabilistic tractography, centrum semiovale, superior longitudinal fasciculus, corpus callosum, cingulum, uncinate fasciculus, fractional anisotropy
- MeSH terms
- Adolescent, Adult, Aged, Aged, 80 and over, Aging, Algorithms, Alzheimer Disease, Brain, Brain Mapping, Cognition Disorders, Female, Humans, Image Processing, Computer-Assisted, Male, Middle Aged, Young Adult, Diffusion Tensor Imaging
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