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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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Cites
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Inter- and intra-individual variation in brain structural-cognition relationships in aging
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Computational anatomy for studying use-dependant brain plasticity
Draganski, B., Kherif, F., & Lutti, A. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00380 · Cited by 37
“…of these issues is subject of recent attempts to correlate in vivo obtained diffusion-tensor derived indices with histology results (Concha et al., 2010; Sagi et al., 2012), resolve interpretational ambiguities (Douaud et al., 2011) and propose novel biophysical models (Zhang et al., 2012).”
BackgroundReduced interhemispheric inhibition in mild cognitive impairment
Tsutsumi, R., Hanajima, R., Hamada, M., Shirota, Y., Matsumoto, H., Terao, Y., Ohminami, S., Yamakawa, Y., Shimada, H., Tsuji, S., et al. (2012) · Experimental Brain Research · doi:10.1007/s00221-011-2997-0 · Cited by 32
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“…preserved in AD, it has been recently acknowledged that there is a benefit in looking at regions where intact and affected fibre tracts are crossing, in order to measure early alterations of white matter that may not be detectable when looking at a fibre tract in isolation (Douaud et al., 2010).”
Schreiber, J., Riffert, T., Anwander, A., & Knösche, T. R. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.01.002 · Cited by 31
“…et al., 2006) has originally been developed to analyze indices derived from the diffusion tensor, but has been extended by Jbabdi and colleagues (Douaud et al., 2011; Jbabdi et al., 2010) to handle direction dependent partial volume fractions (PVF) and, potentially, indices of other…”
Tan, K., Meiri, A., Mowrey, W. B., Abbott, R., Goodrich, J. T., Sandler, A. L., Suri, A. K., Lipton, M. L., & Wagshul, M. E. (2018) · Journal of neurosurgery · doi:10.3171/2017.6.jns162784 · Cited by 32
Multi-Modal Neuroimaging Neural Network-Based Feature Detection for Diagnosis of Alzheimer’s Disease
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“Previous studies had found that the hippocampus of the brain was responsible for human memory and spatial activities and was closely related to AD pathology (Douaud et al., 2011; Fares et al., 2019).”
Scheck, S. M., Pannek, K., Raffelt, D. A., Fiori, S., Boyd, R. N., & Rose, S. (2015) · NeuroImage Clinical · doi:10.1016/j.nicl.2015.09.014 · Cited by 31
“FA results in these regions can be unintuitive and difficult to interpret (Douaud et al., 2011; Pierpaoli et al., 2001).”
Sexual Dimorphism in Healthy Aging and Mild Cognitive Impairment: A DTI Study
O’Dwyer, L., Lamberton, F., Bokde, A. L. W., Ewers, M., Faluyi, Y. O., Tanner, C. J., Mazoyer, B. M., O’Neill, D. J., Bartley, M. M., Collins, R., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037021 · Cited by 30
Impact of brain aging and neurodegeneration on cognition
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Kuceyeski, A. F., Zhang, Y., & Raj, A. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.03.039 · Cited by 32
“…(FA) measured from diffusion MRI data have shown significant findings that are sensitive to early changes, sometimes earlier than gross cortical atrophy is measurable (Avants et al., 2010; Bendlin et al., 2010; Douaud et al., 2011; Gold et al., 2010; Smith et al., 2010; Zhang et al., 2009).”
Podrebarac, S. K., Duerden, E. G., Chau, V., GRUNAU, R. E., Synnes, A. R., Oberlander, T. F., & Miller, S. P. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.11.025 · Cited by 31
“During early development, it is predicted that FA values increase and AD and RD values decrease; however in regions where there is high fiber crossing FA may be artificially increased where crossing fibers are actually declining (Douaud et al., 2011).”
BackgroundMethodDiffusion MRI in acute nervous system injury
Budde, M. D., & Skinner, N. P. (2018) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2018.04.016 · Cited by 31
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“In a recent DTI study of patients with mild cognitive impairment, it was found that both MO and FA increased in the patient group, compared with controls, in the centrum ovale (a region in which association fibres and motor fibres cross) (79).”
BackgroundResultDiffusion tensor imaging in Alzheimer’s disease and affective disorders
Teipel, S. J., Walter, M., Likitjaroen, Y., Schönknecht, P., & Gruber, O. (2014) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-014-0496-6 · Cited by 30
“In contrast, FA along cortico-fugal and cortico-petal fiber tracts was relatively preserved, showing even a relative increase of FA in AD and MCI [36, 148].”
BackgroundInfluentialde Souza, L. C., Lehéricy, S., Dubois, B., Stella, F., & Sarazin, M. (2012) · Current Opinion in Psychiatry · doi:10.1097/yco.0b013e328357b9ab · Cited by 28
“For instance, a recent study with MCI patients demonstrated significant reduction of fractional anisotropy prominently in the anterior corpus callosum [65].”
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Li, Y., Guo, T., Guan, X., Gao, T., Sheng, W., Zhou, C., Wu, J., Xuan, M., Gu, Q., Zhang, M., et al. (2020) · NeuroImage Clinical · doi:10.1016/j.nicl.2020.102355 · Cited by 31
“When differences are detected in voxels of crossing fiber populations, it is difficult to attribute the alterations to specific fiber pathways (Douaud et al., 2011).”
BackgroundGroppa, S., Moeller, F., Siebner, H. R., Wolff, S., Riedel, C. H., Deuschl, G., Stephani, U., & Siniatchkin, M. (2012) · Epilepsia · doi:10.1111/j.1528-1167.2012.03414.x · Cited by 29
“…parameters with increased FA and MD values might correspond consistently with crossing fibers, hypothesizing a selective sparing (or selective degeneration) of one of the pathways or a transition of the white matter to a more linear shape (Pierpaoli et al., 2001; Douaud et al., 2009, 2011).”
BackgroundMishra, V. R., Cheng, H., Gong, G., Yong He, A., Dong, Q., & Huang, H. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00721 · Cited by 29
“…(GFA) (Tuch, 2004; Fritzsche et al., 2010; Zhan et al., 2010), generalized anisotropy (GA) (Ozarslan et al., 2005), mode of anisotropy (Ennis and Kindlmann, 2006; Douaud et al., 2011) and fractions (Hosey et al., 2008; Jbabdi et al., 2010) which are less sensitive to crossing-fiber problem.”
BackgroundTucholka, A., Grau-Rivera, O., Falcon, C., Rami, L., Sánchez-Valle, R., Lladó, A., Gispert, J. D., Molinuevo, J. L., & Initiative, F. T. A. D. N. (2018) · Journal of Alzheimer’s Disease · doi:10.3233/jad-170553 · Cited by 29
“Some previous studies reported that loss of myelination in specific pathways can increase diffusivity in a crossing bundle, and higher axial diffusivity may result in an increase of tracts due to the nature of tractography algorithms [14, 41].”
BackgroundModern Methods for Interrogating the Human Connectome
Lowe, M. J., Sakaie, K., Beall, E. B., Calhoun, V. D., Bridwell, D. A., Rubinov, M., & Rao, S. M. (2016) · Journal of the International Neuropsychological Society · doi:10.1017/s1355617716000060 · Cited by 29
“Reduced FA is typically interpreted as reduced tissue integrity, but has been found to behave counter to expectations in the presence of crossing fibers (Douaud et al., 2011).”
Kelley, S., Plass, J., Bender, A. R., & Polk, T. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab056 · Cited by 30
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“Other MR modalities which can be used for the study of AD include diffusion MRI which measures microstructural changes in white matter [15], functional MRI which measures brain function using BOLD contrast [16], arterial spin labelling which measures the perfusion of blood [17] and MR-relaxometry which characterizes T…”
Disruption of thalamic connectivity in Alzheimer’s disease: a diffusion tensor imaging study
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“found reduced FA and increased MD values in the ATR in mild (MMSE ≥20) to moderate AD (18 ≤MMSE <20) (Douaud et al. 2011).”
BackgroundIn vivo diffusion tensor imaging of amyloid‐β‐induced white matter damage in mice
Sun, S.-W., Liang, H.-F., Mei, J., Xu, D., & Shi, W.-X. (2013) · Journal of Alzheimer s Disease · doi:10.3233/jad-130236 · Cited by 27
“early stage of AD [3–9] and may therefore serve as a marker for early diagnosis and as a potential indicator for treatment efficacy.”
Rowley, J., Fonov, V., Wu, O., Eskildsen, S. F., Schoemaker, D., Wu, L., Mohades, S., Shin, M., Sziklas, V., Cheewakriengkrai, L., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074776 · Cited by 27
“[56,57,65-68] In fact, progression of WM abnormalities has been previously suggested by cross sectional and longitudinal DTI studies [41,42,51,69].”
Perea, R. D. (2013) · Journal of Alzheimer’s Disease & Parkinsonism · doi:10.4172/2161-0460.1000123 · Cited by 30
“In AD, degeneration of the uncinate fasciculus has been associated as a secondary effect after grey matter atrophy [54] and along with the SLF, corpus callosum and cingulum are the fibers most affected [51-55].”
BackgroundMårtensson, J., Lätt, J., Åhs, F., Fredrikson, M., Söderlund, H., Schiöth, H. B., Kok, J., Kremer, B., van Westen, D., Larsson, E.-M., et al. (2018) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2017.03.007 · Cited by 27
Siehl, S., Wicking, M., Pohlack, S. T., Winkelmann, T., Zidda, F., Steiger-White, F., King, J. A., Burgess, N., Flor, H., & Nees, F. (2020) · NeuroImage Clinical · doi:10.1016/j.nicl.2020.102424 · Cited by 29
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“In voxels with multiple and crossing fiber bundles (i.e., complex fiber populations), DTI cannot readily assign differences in white matter to a specific pathway (Douaud et al., 2011; Jones et al., 2013; Mito et al., 2018).”
BackgroundFebo, M., & Foster, T. C. (2016) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2016.00158 · Cited by 28
“Reduced FA is thought to represent WM alterations in aging and pathologies of Alzheimer’s disease in humans (Bozzali et al., 2001; Teipel et al., 2010; Douaud et al., 2011, 2013).”
BackgroundBranzoli, F., Ercan, E., Valabrègue, R., Wood, E. T., Buijs, M., WEBB, A. G., & Ronen, I. (2016) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2016.07.022 · Cited by 29
“Since DTI reflects the molecular diffusion of water, which is present in all tissue compartments, it is influenced by several microstructural factors that affect both the intracellular as well as the extracellular space, including myelin and axonal density, membrane integrity and axonal orientation dispersion (Beaulie…”
BackgroundRojas-Vite, G., Coronado‐Leija, R., Narvaez, O., Ramírez-Manzanares, A., Marroquin, J. L., Noguez-Imm, R., Aranda, M. L., Scherrer, B., Larriva-Sahd, J. A., & Concha, L. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.116013 · Cited by 25
Fixel based analysis of white matter alterations in early stage cerebral small vessel disease
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Contralateral interictal spikes are related to tapetum damage in left temporal lobe epilepsy
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“MO provides measures corresponding to WM fiber complexity (single fiber orientations, multiple fiber orientations or crossings; Douaud et al., 2011).”
BackgroundHigh Angular Resolution Diffusion Imaging
Farquharson, S., & Tournier, J. (2015) · Springer eBooks · doi:10.1007/978-1-4939-3118-7_20 · Cited by 27
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“detecting diffusion changes of complex WM architecture, such as crossing fiber regions [22, 23].”
BackgroundIn search of multimodal brain alterations in Alzheimer's and Binswanger's disease
Fu, Z., Iraji, A., Caprihan, A., Adair, J. C., Jing Sui （Beijing Normal University）， my correct affiliation is beijing normal university, N. Q. U. O. S. A. T., Rosenberg, G. A., & Calhoun, V. D. (2019) · NeuroImage Clinical · doi:10.1016/j.nicl.2019.101937 · Cited by 25
“Similar findings have been reported in previous work on AD (Douaud et al., 2011).”
Brain imaging and human nutrition: which measures to use in intervention studies?
Sizonenko, S. V., Babiloni, C., de Bruin, E. A., Isaacs, E., Jönsson, L. S., Kennedy, D. O., Latulippe, M. E., Mohajeri, M. H., Moreines, J., Pietrini, P., et al. (2013) · British Journal Of Nutrition · doi:10.1017/s0007114513001384 · Cited by 25
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“However, global microstructural changes of white matter are still under investigation in these patients.(20) Studying the process of white matter disruption in MCI and probable mild AD due to AD pathophysiology will increase our understanding of the mechanisms underlying patients’ clinical symptoms as they progress fr…”
BackgroundResultArgyropoulos, G. D., Christidi, F., Karavasilis, E., Velonakis, G., Antoniou, A., Bede, P., Seimenis, I., Kelekis, N., Douzenis, A., Papakonstantinou, O., et al. (2021) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110034 · Cited by 24
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Corpus callosum integrity loss predicts cognitive impairment in Leukoaraiosis
Wang, Z., Bai, L., Liu, Q., Wang, S., Sun, C., Zhang, M., & Zhang, Y. (2020) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.51231 · Cited by 23
“Studies on the white matter microstructure also demonstrated decreasing FA values in the CC in individuals with AD and MCI compared to the HC.(29) In addition, the callosal abnormality was found to be an important predictor of global cognitive impairments in participants with LA.”
ResultMotor pathway degeneration in young ataxia telangiectasia patients: A diffusion tractography study
Sahama, I., Sinclair, K., Fiori, S., Doecke, J. D., Pannek, K., Reid, L. B., Lavin, M. F., & Rose, S. (2015) · NeuroImage Clinical · doi:10.1016/j.nicl.2015.08.007 · Cited by 23
“Indeed, in neurodegenerative conditions, increased anisotropy can be observed in regions of crossing fibers (Douaud et al., 2011), and is observed in average FA magnitude values per bin in the present study.”
Sánchez, S. M., Duarte-Abritta, B., Abulafia, C., Pino, G. D., Bocaccio, H., Castro, M. N., Sevlever, G. E., Fonzo, G. A., Nemeroff, C. B., Gustafson, D., et al. (2020) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2019.12.019 · Cited by 27
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“…uncincate fasciculus and significant increase in radial diffusivity (RD) of left uncinate fasciculus with AD progression [41], increase in FA is found in crossing-fiber regions in MCI and AD and increase is due to the degeneration of secondary fibers in superior longitudinal fasciculus [42].”
Boito, D., Eklund, A., Tisell, A., Levi, R., Özarslan, E., & Blystad, I. (2023) · Brain Communications · doi:10.1093/braincomms/fcad284 · Cited by 26
Steinbach, R., Loewe, K., Kaufmann, J., Machts, J., Kollewe, K., Petri, S., Dengler, R., Heinze, H., Vielhaber, S., Schoenfeld, M. A., et al. (2015) · Journal of Neurology · doi:10.1007/s00415-015-7841-1 · Cited by 22
“, seen in studies on normal aging, mild cognitive impairment or stroke) are a seemingly increased structural integrity caused by a loss of crossing fibers [66–71], a reduction of diffusion barriers due to changes of the neuronal microJ Neurol (2015) 262:2257–2270 2265”
BackgroundWang, P., Chou, K., Lirng, J.-F., Lin, K.-N., Chen, W., & Lin, C. (2012) · Journal of Alzheimer s Disease · doi:10.3233/jad-2012-111304 · Cited by 23
“found that only crossing fibers in the centrum semiovale showed significant anisotrophy changes in aMCI [21].”
InfluentialHespel, A., & Cole, R. C. (2017) · Veterinary Clinics of North America Small Animal Practice · doi:10.1016/j.cvsm.2017.08.002 · Cited by 22
Recent progress in metal–organic frameworks for precaution and diagnosis of Alzheimer’s disease
Liao, Z., Zhang, J., Yu, E., & Cui, Y. (2018) · Polyhedron · doi:10.1016/j.poly.2018.06.013 · Cited by 22
Sullivan, D. R., Logue, M. W., Wolf, E. J., Hayes, J. P., Salat, D. H., Fortier, C. B., Fonda, J. R., McGlinchey, R. E., Milberg, W., & Miller, M. W. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2019.6489 · Cited by 21
Future Directions in Imaging Neurodegeneration
Masdeu, J. C. (2017) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-017-0718-1 · Cited by 22
Genome-wide association studies of brain structure and function in the UK BiobankPreprint
Elliott, L. T., Sharp, K., Alfaro‐Almagro, F., Shi, S., Miller, K. L., Douaud, G., Marchini, J., & Smith, S. M. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/178806 · Cited by 23
Fixel-based analysis reveals tau-related white matter changes in early stages of Alzheimer's disease
Ahmadi, K., Pereira, J. B., Westen, D. V., Pasternak, O., Zhang, F., Nilsson, M., Stomrud, E., Spotorno, N., & Hansson, O. (2024) · The Journal of Neuroscience · doi:10.1523/jneurosci.0538-23.2024 · Cited by 25
Connectome-derived diffusion characteristics of the fornix in Alzheimer's disease
Perea, R. D., Rabin, J. S., Fujiyoshi, M. G., Neal, T. E., Smith, E. E., Dijk, K. R. A. V., & Hedden, T. (2018) · NeuroImage Clinical · doi:10.1016/j.nicl.2018.04.029 · Cited by 20
“…fiber tracts, findings of higher axial diffusivity in Alzheimer's disease have been postulated to reflect a reduction of crossing fibers that results in a higher principal axis of diffusion because fibers running in other directions are no longer present (Douaud et al., 2011; Teipel et al., 2014).”
Martin, J., Endt, S., Wetscherek, A., Kuder, T. A., Doerfler, A., Uder, M., Hensel, B., & Laun, F. B. (2019) · Zeitschrift für Medizinische Physik · doi:10.1016/j.zemedi.2019.01.003 · Cited by 21
Gutman, D. A., Magnuson, M. E., Majeed, W., Keifer, O. P., Davis, M., Ressler, K. J., & Keilholz, S. D. (2012) · Brain Structure and Function · doi:10.1007/s00429-012-0413-6 · Cited by 21
“DTI has been extensively used in both human (Douaud et al. 2011; Gutman et al. 2009; Wedeen et al. 2008) and primate studies (Li et al.”
Liang, Y., Li, H., Lv, C., Shu, N., Chen, K., Li, X., Zhang, J., Hu, L., & Zhang, Z. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.1 · Cited by 20
“Increased MD was reported to be caused by decrease in membrane density and DA could reflect the axonal injury (Douaud et al, 2011; Wheeler-Kingshott and Cercignani, 2009).”
Reduced white matter integrity in amateur boxers
Herweh, C., Hess, K., Meyding‐Lamadé, U., Bartsch, A. J., Stippich, C., Jost, J., Friedmann‐Bette, B., Heiland, S., Bendszus, M., & Hähnel, S. (2016) · Neuroradiology · doi:10.1007/s00234-016-1705-y · Cited by 21
Diffusion Tensor Imaging in the Study of Aging and Age-Associated Neural Disease
Salat, D. H. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-396460-1.00012-3 · Cited by 21
Fiber-specific white matter alterations in early-stage tremor-dominant Parkinson’s disease
Andica, C., Kamagata, K., Saito, Y., Uchida, W., Fujita, S., Hagiwara, A., Akashi, T., Wada, A., Ogawa, T., Hatano, T., et al. (2021) · npj Parkinson's Disease · doi:10.1038/s41531-021-00197-4 · Cited by 21
Zhao, H., Cheng, J., Liu, T., Jiang, J., Koch, F. C., Sachdev, P. S., Basser, P. J., Wen, W. X., & Initiative, A. D. N. (2021) · Human Brain Mapping · doi:10.1002/hbm.25628 · Cited by 19
“This is consistent with previous reports on the pattern of microstructural white matter damages in AD (Benitez et al., 2014; Douaud et al., 2011; Mayo, Mazerolle, Ritchie, Fisk, & Gawryluk, 2017).”
Sali, D., Verganelakis, D. A., Gotsis, E. D., Toulas, P., Papatriantafillou, J., Karageorgiou, C. E., Thomaides, T., Kapsalaki, E. Z., Hadjigeorgiou, G. M., & Papadimitriou, A. (2013) · Acta Neurologica Belgica · doi:10.1007/s13760-013-0197-3 · Cited by 20
“Previous studies have also shown abnormal integrity of SLF in MCI and AD [11, 24, 27, 36].”
ResultRelation between aerobic fitness and brain structures in amnestic mild cognitive impairment elderly
Teixeira, C. V. L., de Rezende, T. J. R., Weiler, M., Nogueira, M. H., de Campos, B. M., Pegoraro, L., Vicentini, J. E., Braz, G. S., Cendes, F., & Balthazar, M. L. F. (2016) · AGE · doi:10.1007/s11357-016-9912-3 · Cited by 21
“That said, the macrostructural changes that have been reported to occur in the brain—such as volume loss and cortical thinning— are likely a result from subtler microscopic changes in the cerebral tissue (Douaud et al. 2011).”
BackgroundUnveiling causal relationship between white matter tracts and psychiatric disorders
Yu, Y., Jia, T., Lin, X., Bao, Y., Chang, S., Sun, J., Gao, T., Shi, J., Ai, S., & Yuan, K. (2025) · Communications Biology · doi:10.1038/s42003-025-08669-6 · Cited by 20
“Althoughimaging indicators are indirect proxies, current studies tend to interpret decreases in FA and increases in MD as indicators of white matter myelin integrity damage 6,7 or axonal damage 8 .”
Guberman, G. I., Houde, J.-C., Ptito, A., Gagnon, I., & Descoteaux, M. (2019) · Brain Structure and Function · doi:10.1007/s00429-019-02002-8 · Cited by 17
Yao, Z., Sligte, I. G., Moreau, D., Hsieh, S., Yang, C.-T., Ridderinkhof, K. R., Muggleton, N. G., & Wang, C. (2020) · Cortex · doi:10.1016/j.cortex.2020.07.016 · Cited by 21
Extreme capsule is a bottleneck for ventral pathway
Shekari, E., Goudarzi, S., Shahriari, E., & Joghataei, M. T. (2021) · IBRO Neuroscience Reports · doi:10.1016/j.ibneur.2020.11.002 · Cited by 19
“These results show that in addition to the association fibers between the hemispheres, examining the ventral pathway can be a helpful marker in diagnosing cognitive impairment (Douaud et al., 2011).”
ResultNir, T. M., Jahanshad, N., Jack, C. R., Weiner, M. W., Toga, A. W., & Thompson, P. M. (2012) · IEEE International Symposium on Biomedical Imaging (ISBI) · doi:10.1109/isbi.2012.6235831 · Cited by 19
“Such patterns have also been found in other studies of elderly patients [22].”
ResultOverview + Detail Visualization for Ensembles of Diffusion Tensors
Zhang, C., Caan, M. W. A., Höllt, T., Eisemann, E., & Vilanova, A. (2017) · Computer Graphics Forum · doi:10.1111/cgf.13173 · Cited by 19
Qi, X., Du, Z. J., Zhu, L., Liu, X., Xu, H., Zhou, Z., Zhong, C., Li, S., Wang, L., & Zhang, Z. (2019) · Neuroscience Bulletin · doi:10.1007/s12264-018-0325-4 · Cited by 19
Jiang, M., Wen, Z., Long, L., Wong, C. W., Ye, N., Zee, C., & Chen, B. T. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00597 · Cited by 20
“DTI is an established magnetic resonance imaging (MRI) method that measures the directionality of water diffusion in the brain and is more sensitive for detecting WM microstructural alterations than volumetric methods (Douaud et al., 2011).”
MethodMeasuring Restriction Sizes Using Diffusion Weighted Magnetic Resonance Imaging: A Review
Martin, M. (2013) · Magnetic Resonance Insights · doi:10.4137/mri.s11149 · Cited by 19
Brain tissue modifications induced by cholinergic therapy in Alzheimer's disease
Bozzali, M., Parker, G. J. M., Spanò, B., Serra, L., Giulietti, G., Perri, R., Magnani, G., Marra, C., Vita, M. G., Caltagirone, C., et al. (2012) · Human Brain Mapping · doi:10.1002/hbm.22130 · Cited by 19
“An alternative explanation is provided with reference to a recent study by another group [Douaud et al., 2011], investigating the ‘‘mode of anisotropy,’’ an index reflecting how ‘‘linear’’ (as opposed to ‘‘planar’’) the shape of diffusion tensor is in a voxel.”
ResultStructural disconnectivity and the risk of dementia in the general population
Cremers, L. G. M., Wolters, F. J., de Groot, M., Ikram, M. A., van der Lugt, A., Niessen, W. J., Vernooij, M. W., & Ikram, M. A. (2020) · Neurology · doi:10.1212/wnl.0000000000010231 · Cited by 18
“Lower FA values in limbic system tracts (in particular in the parahippocampal cingulum) and the association with dementia, more specifically AD, has been most consistently reported in previous studies.40,42,43 A small number of studies reported higher FA values in specific regions in AD.44,45 This counterintuitive fin…”
BackgroundOttoy, J., Ozzoude, M., Zukotynski, K., Kang, M. S., Adamo, S. M., Scott, C. J. M., Ramirez, J., Swardfager, W., Lam, B., Bhan, A., et al. (2023) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x231152001 · Cited by 18
“46,47 Second, we observed, similar to prior work, that cortical and NAWM SUVRs are positively correlated even after partial volume correction/erosion.”
Tsao, S., Gajawelli, N., Zhou, J., Shi, J., Ye, J., Wang, Y., & Leporé, N. (2017) · Brain and Behavior · doi:10.1002/brb3.733 · Cited by 18
“…et al., 2001; Choi, Lim, & Monteiro, 2005; Chua, Wen, & Slavin, 2008; Clerx, Visser, Verhey, & Aalten, 2012; Concha, Gross, & Beaulieu, 2005; Douaud et al., 2011; Frisoni, Fox, Jack, & Scheltens, 2010; Jack, Bernstein, & Fox, 2008; Jahng et al., 2011; Lo, Wang, Chou, & Wang, 2010; Nakata et…”
Inhaled Xenon Washout as a Biomarker of Alzheimer’s Disease
Hane, F. T., Li, T., Plata, J. A., Hassan, A. A., Granberg, K., & Albert, M. S. (2018) · Diagnostics · doi:10.3390/diagnostics8020041 · Cited by 20
Leeuwis, A. E., Weaver, N. A., Biesbroek, J. M., Exalto, L. G., Kuijf, H. J., Hooghiemstra, A. M., Prins, N. D., Scheltens, P., Barkhof, F., van der Flier, W. M., et al. (2019) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.180136 · Cited by 18
“As the CST is located in an area with crossing fasciculi (i.e. the superior longitudinal fasciculus), these results measured with DTI may be interpreted with caution (36).”
BackgroundTermenón, M., Graña, M., Besga, A., Echeveste, J., & González-Pinto, A. M. (2012) · Neurocomputing · doi:10.1016/j.neucom.2012.08.044 · Cited by 18
In vivo assessment of use-dependent brain plasticity—Beyond the “one trick pony” imaging strategy
Draganski, B., & Kherif, F. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.08.058 · Cited by 20
“Importantly, there are recent attempts to correlate in vivo obtained diffusion-tensor derived indices with histology results (Concha et al., 2010) and resolve interpretational issues (Douaud et al., 2011).”
Diffusion MRI in Neurological Disorders
Bodini, B., & Ciccarelli, O. (2009) · Elsevier eBooks · doi:10.1016/b978-0-12-374709-9.00009-2 · Cited by 18
Multimodal MRI quantification of the common neurostructural bases within the FTD-ALS continuum
Crespi, C., Dodich, A., Cappa, S. F., Canessa, N., Iannaccone, S., Corbo, M., Lunetta, C., Falini, A., & Cerami, C. (2017) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2017.09.019 · Cited by 17
“Despite the intrinsic heterogeneity of the ALS population, the d generation of these WM tracts has been consistently observed in several DTI investigations (e.g., Douaud et al., 2011a; Filippini et al., 2010; Turner et al., 2012), and reported in some neuropathological studies (e.g., Smith, 1960).”
You, P., Li, X., Wang, Z., Wang, H., Dong, B., & Li, Q. (2021) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2021.654381 · Cited by 17
Sun, J., Zhu, Z., Chen, K., Wei, D., Li, X., Li, H., Zhang, J., Chen, X., Chen, Y., & Zhang, Z. (2020) · Aging · doi:10.18632/aging.103367 · Cited by 16
Analysis of longitudinal diffusion-weighted images in healthy and pathological aging: An ADNI study
Kruggel, F., Masaki, F., & Solodkin, A. (2017) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2016.12.020 · Cited by 16
“…is documented that metrics based n DWI have high sensitivity for detecting AD-related WM changes Amlien and Fjell, 2014; Bennett et al., 2010; Douaud et al., 2011; uang et al., 2012; Kantarci et al., 2005; Keihaninejad et al., 2013; alat et al., 2010; Teipel et al., 2010, 2014; Wang et al.,…”
BackgroundInfluentialZajac, L., Koo, B., Bauer, C. M., Killiany, R., & Initiative, B. O. T. A. D. N. (2017) · Brain Sciences · doi:10.3390/brainsci7040037 · Cited by 17
Timmermans, C., Smeets, D., Verheyden, J., Terzopoulos, V., Anania, V., Parizel, P. M., & Maas, A. I. R. (2019) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.26333 · Cited by 16
“In this way, researchers were able to detect, among others, axonal recovery in some patients with traumatic brain injury and to predict prodromal Alzheimer’s disease in subjects with mild cognitive impairment.(6,7) Yet despite its promise, the use of DTI in longitudinal or multicenter research studies has been limited.”
ResultSrisaikaew, P., Wongpakaran, N., Anderson, N. D., Chen, J. J., Kothan, S., Varnado, P., Unsrisong, K., & Mahakkanukrauh, P. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.594002 · Cited by 16
Brain-wide structural connectivity alterations under the control of Alzheimer risk genes
Shen, L., Goñi, J., Saykin, A. J., Wu, Y. C., Fang, S., Sporns, O., Amico, E., Yan, J., Nho, K. T., Huang, Z., et al. (2020) · International Journal of Computational Biology and Drug Design · doi:10.1504/ijcbdd.2020.10026789 · Cited by 15
Han, A., Dhollander, T., Sun, Y., Chad, J. A., & Chen, J. J. (2023) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2023.06.007 · Cited by 17
BootGraph: Probabilistic fiber tractography using bootstrap algorithms and graph theory
Vorburger, R. S., Reischauer, C., & Boesiger, P. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.10.058 · Cited by 16
“For example, ongoing studies in the field of aging and neurodegenerative diseases, such as mild cognitive impairment or dementia including Alzheimer's disease, are based on DTI (Bozzali et al., 2012; Douaud et al., 2011; Lo et al., 2010).”
BackgroundChad, J. A., Pasternak, O., & Chen, J. J. (2021) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2020.12.020 · Cited by 12
Shirazi, Y., Oghabian, M., & Batouli, S. A. H. (2021) · Clinical neurology and neurosurgery (Dutch-Flemish ed. Print) · doi:10.1016/j.clineuro.2021.107048 · Cited by 13
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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