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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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Citations
Cites
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“05, corrected for multiple comparisons using the “2D” parameter settings with threshold-free cluster enhancement (TFCE), a method which avoids using an arbitrary threshold for the initial cluster-formation (Smith and Nichols, 2009).”
MethodInfluentialWinblad, B., Palmer, K., Kivipelto, M., Jelic, V., Fratiglioni, L., Wahlund, L. ‐., Nordberg, A., Bäckman, L., Albert, M., Almkvist, O., et al. (2004) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2004.01380.x · Cited by 4,946 · cited 2×
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Cited by
Sorted by citations
Items 101–200 of 514
Musical training induces functional and structural auditory‐motor network plasticity in young adults
Li, Q., Wang, X., Wang, S., Xie, Y., Li, X., Xie, Y., & Li, S. (2018) · Human Brain Mapping · doi:10.1002/hbm.23989 · Cited by 92
“Increases in FA are thought to be associated with changes in axon diameter, the fanning of primary fibers or the density and coherence of secondary fibers in crossing regions (Douaud et al., 2009, 2011; Zatorre, Fields, & Johansen-Berg, 2012).”
BackgroundMemory binding and white matter integrity in familial Alzheimer’s disease
Parra, M. A., Saarimäki, H., Bastin, M. E., Londoño, A. C., Pettit, L., Lopera, F., Della Sala, S., & Abrahams, S. (2015) · Brain · doi:10.1093/brain/awv048 · Cited by 79
Yip, S. W., Morie, K. P., Xu, J., Constable, R. T., Malison, R. T., Carroll, K. M., & Potenza, M. N. (2016) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2016.03.001 · Cited by 80
“Pre-processing and diffusion estimates—dMRI data were analyzed in FSL using recommended tract-based spatial statistics (TBSS) procedures (26, 30, 49): dMRI acquisitions (two per participant) were corrected for gradient coil eddy currents and head movement using affine registration (46, 49).”
MethodMolinuevo, J. L., Ripollés, P., Simó, M., Lladó, A., Olives, J., Balasa, M., Antonell, A., Rodríguez‐Fornells, A., & Rami, L. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.05.027 · Cited by 82
Dance and music training have different effects on white matter diffusivity in sensorimotor pathways
Giacosa, C., Karpati, F. J., Foster, N. E. V., Penhune, V. B., & Hyde, K. L. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.04.048 · Cited by 88
“More specifically, lower MO was found in dancers' projection fibres (especially the CST), association fibres (SLF), and some ventral prefrontal regions.”
InfluentialYang, C., Zhong, S., Zhou, X., Wei, L., Wang, L., & Nie, S. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00261 · Cited by 77
“…MRI is the only non-invasive neuroimaging technique that can provide exquisite details of WM fiber bundles in vivo, and have been extensively applied to study AD and MCI (Douaud et al., 2011; Liu et al., 2011; Bosch et al., 2012; Huang et al., 2012; Voineskos et al., 2012; Amlien and Fjell, 2014).”
BackgroundAndersen, K. W., Lasič, S., Lundell, H., Nilsson, M., Topgaard, D., Sellebjerg, F. T., Szczepankiewicz, F., Siebner, H. R., Blinkenberg, M., & Dyrby, T. B. (2020) · Brain Communications · doi:10.1093/braincomms/fcaa077 · Cited by 77
“On the other hand, axonal degeneration of a single fibre bundle in a crossing-fibre region may reduce the regional dispersion of fibre orientation dispersion and hereby increase regional FA (Pierpaoli et al., 2001; Douaud et al., 2011; Teipel et al., 2014).”
BackgroundMapping white matter integrity in elderly people with HIV
Nir, T. M., Jahanshad, N., Busovaca, E., Wendelken, L. A., Nicolas, K., Thompson, P. M., & Valcour, V. (2013) · Human Brain Mapping · doi:10.1002/hbm.22228 · Cited by 79
“This pattern has been found in other studies of elderly patients with a neurodegenerative disorder, and may reflect a selective sparing or selective degeneration of one of the pathways in a region of crossing fibers (Douaud et al., 2011).”
ResultLongitudinal changes in white matter microstructure after heavy cannabis use
Becker, M. P., Collins, P. F., Lim, K. O., Muetzel, R. L., & Luciana, M. M. (2015) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2015.10.004 · Cited by 82
“…fiber population, i.e., during development within a parallel bundled tract, while the converse (FA decreases) may be observed when neural development occurs within multiple fiber populations in the same region, i.e., areas where fibers cross or fan out into gray matter (e.g., Douaud et al., 2011).”
BackgroundHahn, C., Lim, H.-K., Won, W. Y., Ahn, K. J., Jung, W.-S., & Lee, C. U. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053493 · Cited by 76
“[53] reported that WM microstrudtural changes in the cingulum, uncinate fasciculus, corpus callosum and superior longitudinal fasciculus were observed in patients with AD.”
BackgroundAlves, G. S., Knöchel, V. O., Knöchel, C., Carvalho, A. F., Pantel, J., Engelhardt, E., & Laks, J. (2015) · BioMed Research International · doi:10.1155/2015/291658 · Cited by 78
“Other biomarkers of risk to dementia, such as the presence of ApoE4 and inflammatory markers (IL6, CRP), may be associated with a steeper decline on cognitive status or greater neuronal loss [79].”
BackgroundSzczepankiewicz, F., Lätt, J., Wirestam, R., Leemans, A., Sundgren, P. C., van Westen, D., Ståhlberg, F., & Nilsson, M. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.02.078 · Cited by 72
“An example of this may be found in Alzheimer's disease, where the FA unexpectedly increases in areas of crossing fibers, probably due to the removal of one fiber population (Douaud et al., 2011).”
Williams, V. J., Leritz, E. C., Shepel, J., McGlinchey, R. E., Milberg, W., Rudolph, J. L., Lipsitz, L. A., & Salat, D. H. (2012) · Human Brain Mapping · doi:10.1002/hbm.22030 · Cited by 74
“Recently, the mode of anisotropy has been introduced as a useful DTI parameter in determining voxels containing crossing fibers [Douaud et al., 2011], and we plan to further investigate this measure in an upcoming manuscript focusing on multispectral signatures of white matter pathology related to…”
BackgroundData-Driven Subtyping of Executive Function–Related Behavioral Problems in Children
Bathelt, J., Holmes, J., Astle, D. E., Holmes, J., Gathercole, S., Astle, D., Manly, T., & Kievit, R. (2018) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2018.01.014 · Cited by 71
Early deprivation, atypical brain development, and internalizing symptoms in late childhood
Bick, J. R., Fox, N. A., Zeanah, C. H., & Nelson, C. A. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.09.026 · Cited by 76
“Considering the ages of participants in the BEIP (between 8 and 10 years at the time of the scan), a study-specific FA template in the standard space, instead of the FMRIB_FA_58 adult brain template, was created in a two-step approach (Douaud et al., 2011) for the TBSS analysis in this study.”
MethodSahara, N., Perez, P. D., Lin, W.-L., Dickson, D. W., Ren, Y., Zeng, H., Lewis, J., & Febo, M. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2013.12.009 · Cited by 70
“…ranges quantitatively from 1 for a planar or “pancake-like” diffusion ellipsoid (expected from regions containing crossing fibers for diffusion in 2 dimensions) to a value ofþ1 for a linear or “cigar-like” ellipsoid expected from predominantly single fiber tract areas (Douaud et al., 2011, 2013).”
InfluentialZhang, B., Xu, Y., Zhu, B., & Kantarci, K. (2013) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.12166 · Cited by 70
“NC ST-TBSS[53,60] SS-TBSS[57] VBA-SPM8[79] MD+ FA+/ MD+ FA+ MD+ FA+ MD+ FA+ MD+ FA+ FA reduction: uncinate fasciculus, brain stem, cerebellum[53,60] MD increases: occipitofrontal fasciculi, superior longitudinal fasciculus, callosal body, uncinate fasciculus[53,57,79] AD vs.”
BackgroundSantis, S. D., Barazany, D., Jones, D. K., & Assaf, Y. (2015) · Magnetic Resonance in Medicine · doi:10.1002/mrm.25644 · Cited by 66
Associations between T1 white matter lesion volume and regional white matter microstructure in aging
Leritz, E. C., Shepel, J., Williams, V. J., Lipsitz, L. A., McGlinchey, R. E., Milberg, W., & Salat, D. H. (2013) · Human Brain Mapping · doi:10.1002/hbm.22236 · Cited by 68
“, 2012), and regional patterns of this degeneration differ from abnormal conditions such as Alzheimer’s disease (Damoiseaux et al., 2009; Douaud et al., 2011; Huang et al., 2011; Salat et al., 2010), cerebral amyloid angiopathy (Salat et al.”
BackgroundLong term motor function after neonatal stroke: Lesion localization above all
Dinomais, M., Hertz‐Pannier, L., Groeschel, S., Chabrier, S., Delion, M., Husson, B., Kossorotoff, M., Renaud, C., Tich, S. N. T., & for the AVCnn Study Group (2015) · Human Brain Mapping · doi:10.1002/hbm.22950 · Cited by 64
“In this complex crossing-fiber region, tissue damage can result in lower or higher FA [Douaud et al., 2011; Groeschel et al., 2014] and axial and radial diffusivities may not be meaningful [Wheeler-Kingshott and Cercignani, 2009].”
BackgroundAlves, G. S., O’Dwyer, L., Jurcoane, A., Oertel‐Knöchel, V., Knöchel, C., Prvulovic, D., Sudo, F. K., Alves, C. E. D. O., Valente, L., Moreira, D., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0052859 · Cited by 70
“Nevertheless, studies with a similar MRI technology reported diffusions changes in many analogous WM tracts as ours [63–65]; recent evidence with probabilistic tractography, which allows to trace pathways from crossing-fiber regions, also give support to our findings, by evidencing that the SLF, UF, corpus callosum (e…”
ResultAdvances in MRI Biomarkers for the Diagnosis of Alzheimer’s Disease
Kehoe, E. G., McNulty, J. P., Mullins, P. G., & Bokde, A. L. W. (2014) · Biomarkers in Medicine · doi:10.2217/bmm.14.42 · Cited by 70
Gray and white matter degeneration revealed by diffusion in an Alzheimer mouse model
Zerbi, V., Kleinnijenhuis, M., Fang, X., Jansen, D., Veltien, A., Van Asten, J., Timmer, N., Dederen, P. J., Kiliaan, A. J., & Heerschap, A. (2013) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2012.11.017 · Cited by 74
“This concept has been discussed recently for AD patients, in whom the increase of FA in crossing-fiber areas was associated with early white matter alterations (Douaud et al., 2011).”
BackgroundFractional Anisotropy changes in Parahippocampal Cingulum due to Alzheimer’s Disease
da Rocha, J. L. D., Bramati, I. E., Coutinho, G., Tovar-Moll, F. F., & Sitaram, R. (2020) · Scientific Reports · doi:10.1038/s41598-020-59327-2 · Cited by 61
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“The diffusion MRI data were corrected for distortions, eddy currents and head motion and then modeled using FMRIB’s Diffusion Toolbox for diffusion modeling and tractography analysis 105,106 .”
Bender, A. R., & Raz, N. (2015) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2015.02.001 · Cited by 65
“Thus, controlling for such influences (Douaud et al., 2011) may bolster inferential speculation about spatial patterns of RD and AD and correspondence with underlying cellular or pathological processes associated with aging.”
BackgroundWhite matter and memory in healthy adults: Coupled changes over two years
Bender, A. R., Prindle, J., Brandmaier, A. M., & Raz, N. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.10.085 · Cited by 61
“…traditional single tensormodels (withmuch greater number of gradient directions) to better understand the relationships between the DTI indices reported for the last 15 years and the presence and influence of crossing fibers (De Santis et al, 2014; Douaud et al., 2011; Ennis and Kindlmann, 2006).”
White matter microstructure is altered in cognitively normal middle-aged APOE-ε4 homozygotes
Study, F. T. A., Operto, G., Cacciaglia, R., Grau‐Rivera, O., Falcón, C., Brugulat‐Serrat, A., Ródenas, P., Ramos, R., Morán, S., Esteller, M., et al. (2018) · Alzheimer s Research & Therapy · doi:10.1186/s13195-018-0375-x · Cited by 61
Structural correlates of skilled performance on a motor sequence task
Steele, C. J., Scholz, J., Douaud, G., Johansen‐Berg, H., & Penhune, V. B. (2012) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2012.00289 · Cited by 62
“However, because axial and radial diffusivity are defined relative to the axis of greatest diffusivity, rather than to particular tracts, their interpretation is non-trivial in a complex human brain with multiple fiber crossings (Jbabdi et al., 2010; Douaud et al., 2011).”
BackgroundInfluentialSmith, J. C., Lancaster, M. A., Nielson, K. A., Woodard, J. L., Seidenberg, M., Durgerian, S., Sakaie, K., & Rao, S. M. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.08.007 · Cited by 60
“These effects are consistentwith selective degenerative processes that preserve the tract along its primary longitudinal axis (Douaud et al., 2011).”
InfluentialNeuroanatomical correlates of verbal fluency in early Alzheimer’s disease and normal aging
Rodríguez‐Aranda, C., Waterloo, K. K., Johnsen, S. H., Eldevik, P., Sparr, S., Wikran, G., Herder, M., & Vangberg, T. R. (2016) · Brain and Language · doi:10.1016/j.bandl.2016.03.001 · Cited by 57
White Matter Differences Among Adolescents Reporting Psychotic Experiences
O’Hanlon, E., Leemans, A., Kelleher, I., Clarke, M. C., Roddy, S., Coughlan, H., Harley, M., Amico, F., Hoscheit, M. J., Tiedt, L., et al. (2015) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2015.0137 · Cited by 57
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T1 relaxometry of crossing fibres in the human brain
Santis, S. D., Assaf, Y., Jeurissen, B., Jones, D., & Roebroeck, A. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.07.037 · Cited by 55
Nedelská, Z., Schwarz, C. G., Boeve, B. F., Lowe, V. J., Reid, R. I., Przybelski, S. A., Lesnick, T. G., Gunter, J. L., Senjem, M. L., Ferman, T. J., et al. (2015) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2015.03.007 · Cited by 52
“Hence, FA is often used as a proxy of WM integrity (Carmichael and Lockhart, 2012; Douaud et al., 2011).”
Lista, S., Molinuevo, J. L., Cavedo, E., Rami, L., Amouyel, P., Teipel, S. J., Garaci, F., Toschi, N., Habert, M.-O., Blennow, K., et al. (2015) · Journal of Alzheimer's Disease · doi:10.3233/jad-150202 · Cited by 53
Xu, B., Sandrini, M., Wang, W., Smith, J. F., Sarlls, J. E., Awosika, O. O., Butman, J. A., Horwitz, B., & Cohen, L. G. (2016) · Human Brain Mapping · doi:10.1002/hbm.23236 · Cited by 53
“, 2015], particularly the crossing fiber issue that would likely influence the DTI tractography, fiber counts, and FA measurements [Douaud et al., 2011].”
BackgroundMethodThe DELCODE Study Group, Brueggen, K., Dyrba, M., Cardenas-Blanco, A., Schneider, A., Fliessbach, K., Buerger, K., Janowitz, D., Peters, O., Menne, F., et al. (2019) · Journal of Neurology · doi:10.1007/s00415-019-09429-3 · Cited by 51
Caballero, M. Á. A., Song, Z., Rubinski, A., Duering, M., Dichgans, M., Park, D. C., & Ewers, M. (2020) · Alzheimer s & Dementia · doi:10.1002/alz.12062 · Cited by 52
3 D tract‐specific local and global analysis of white matter integrity in A lzheimer's disease
Jin, Y., Huang, C., Daianu, M., Zhan, L., Dennis, E. L., Reid, R. I., Jack, C. R., Hongtu Zhu, B., Thompson, P. M., & Initiative, A. D. N. (2016) · Human Brain Mapping · doi:10.1002/hbm.23448 · Cited by 50
“As the CST is involved in control of motor function of the body, only a few studies have analyzed the tract so far [Douaud et al., 2011; Teipel et al., 2007].”
BackgroundStructural network differences in chronic musculoskeletal pain: Beyond fractional anisotropy
Bishop, J. H., Shpaner, M., Kubicki, A., Clements, S., Watts, R., & Naylor, M. R. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.12.021 · Cited by 50
“MO provides measures corresponding to WM fiber complexity by defining whether anisotropy is linear, such as in the case of single fiber orientations, or planar, which is indicative of multiple fiber orientations or crossings (Douaud et al., 2011; Ennis and Kindlmann, 2006).”
Magnetic resonance imaging and histology correlation in the neocortex in temporal lobe epilepsy
Goubran, M., Hammond, R. R., de Ribaupierre, S., Burneo, J. G., Mirsattari, S. M., Steven, D. A., Parrent, A. G., Peters, T. M., & KHAN, A. R. (2014) · Annals of Neurology · doi:10.1002/ana.24318 · Cited by 48
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“Another study also found significant abnormalities in a crossing fiber region known as the centrum semiovale (close to an important hub region, [6]) only in MCI patients compared to cognitively healthy age-matched controls [39].”
ResultDoan, N. T., Engvig, A., Persson, K., Alnæs, D., Kaufmann, T., Rokicki, J., Córdova‐Palomera, A., Moberget, T., Brækhus, A., Barca, M. L., et al. (2017) · Scientific Reports · doi:10.1038/srep45131 · Cited by 52
Altered white matter microstructure in lupus patients: a diffusion tensor imaging study
Nystedt, J., Nilsson, M., Jönsen, A., Nilsson, P., Bengtsson, A. A., Lilja, Å., Lätt, J., Mannfolk, P., & Sundgren, P. C. (2018) · Arthritis Research & Therapy · doi:10.1186/s13075-018-1516-0 · Cited by 48
Progressive white matter changes following anterior temporal lobe resection for epilepsy
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“…the interpretation of the observed postoperative increases in FA as selective degeneration of a single fiber population from two crossing fiber populations in the corona radiata has previously been shown to lead to a paradoxical rise in FA in patients with Alzheimer's disease (Douaud et al., 2011).”
BackgroundShen, X., Adams, M. J., Ritakari, T. E., Cox, S. R., McIntosh, A. M., & Whalley, H. C. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.06.011 · Cited by 48
Effect of aerobic exercise on white matter microstructure in the aging brain
Clark, C. M., Guadagni, V., Mazerolle, E. L., Hill, M. D., Hogan, D. B., Pike, G. B., & Poulin, M. J. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112042 · Cited by 47
Illa, M., Eixarch, E., Batallé, D., Arbat‐Plana, A., Muñoz‐Moreno, E., Figueras, F., & Gratacós, E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0076453 · Cited by 46
Curran, K. M., Emsell, L., & Leemans, A. (2015) · Springer eBooks · doi:10.1007/978-1-4939-3118-7_5 · Cited by 45
The contribution of brain imaging to the understanding of psychopathy
Pujol, J., Harrison, B. J., Contreras‐Rodríguez, O., & Cardoner, N. (2018) · Psychological Medicine · doi:10.1017/s0033291718002507 · Cited by 52
“Accordingly, from early adulthood, the normal physiological evolution of FA is one of the progressive reductions, presumably reflecting increased white matter structural complexity accompanying brain maturation (Douaud et al., 2011; Jones et al., 2013).”
BackgroundBuono, V. L., Palmeri, R., Corallo, F., Allone, C., Pria, D., Bramanti, P., & Marino, S. (2019) · International Journal of Neuroscience · doi:10.1080/00207454.2019.1667798 · Cited by 48
“Also the fornix appeared severe affected in preclinical stage of AD, suggesting that it should be selectively more vulnerable than other limbic WM tracts [18,23,32].”
BackgroundHe, Q., Turel, O., & Bechara, A. (2018) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2018.06.008 · Cited by 48
Matthews, P. M., Filippini, N., & Douaud, G. (2012) · Journal of Alzheimer s Disease · doi:10.3233/jad-2012-129012 · Cited by 46
Gutman, D. A., Keifer, O. P., Magnuson, M. E., Choi, D. C., Majeed, W., Keilholz, S. D., & Ressler, K. J. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.07.014 · Cited by 43
“DTI has also been extensively used in both human (Douaud et al., 2011; Gutman et al., 2009; Wedeen et al., 2008) and primate studies (Li et al.”
Structural abnormality of the corticospinal tract in major depressive disorder
Sacchet, M. D., Prasad, G., Foland‐Ross, L. C., Joshi, S. H., Hamilton, J. P., Thompson, P. M., & Gotlib, I. H. (2014) · Biology of Mood & Anxiety Disorders · doi:10.1186/2045-5380-4-8 · Cited by 44
“found that the increases in CST FA were associated with reduced FA of SLF association fibers in a crossing fiber region at the level of the centrum semiovale [33].”
BackgroundNusbaum, F., Hannoun, S., Kocevar, G., Stamile, C., Fourneret, P., Revol, O., & Sappey‐Marinier, D. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00173 · Cited by 50
Hanaie, R., Mohri, I., Kagitani‐Shimono, K., Tachibana, M., Matsuzaki, J., Watanabe, Y., Fujita, N., & Taniike, M. (2014) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-014-2096-8 · Cited by 42
“Previous studies suggested that regions with crossing fibers showed lower or higher FA (Douaud et al. 2011; Lebel et al. 2010).”
ResultThe Corticospinal Tract in Huntington's Disease
Phillips, O. R., Squitieri, F., Sánchez‐Castañeda, C., Elifani, F., Griguoli, A. M., Maglione, V., Caltagirone, C., Sabatini, U., & Paola, M. D. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhu065 · Cited by 41
“…understood (for an in-depth discussion of diffusion imaging see Jones et al. 2013), and interpretation should keep in mind the underlying WM anatomy and possible tract-specific neuropathology (Douaud et al. 2011), it is agreed that this approach is sensitive to microstructural tissue properties.”
BackgroundThe pathophysiology of episodic cluster headache: Insights from recent neuroimaging research
Yang, F., Chou, K., Kuo, C.-Y., Lin, Y., Lin, C., & Wang, S. (2017) · Cephalalgia · doi:10.1177/0333102417716932 · Cited by 42
Svärd, D., Nilsson, M., Lampinen, B., Lätt, J., Sundgren, P. C., Stomrud, E., Minthon, L., Hansson, O., & van Westen, D. (2017) · PLoS ONE · doi:10.1371/journal.pone.0185239 · Cited by 45
Operto, G., Molinuevo, J. L., Cacciaglia, R., Falcon, C., Brugulat-Serrat, A., Suárez-Calvet, M., Grau-Rivera, O., Bargalló, N., Morán, S., Esteller, M., et al. (2019) · NeuroImage: Clinical · doi:10.1016/j.nicl.2019.101983 · Cited by 40
Structural hippocampal network alterations during healthy aging: a multi-modal MRI study
Pelletier, A., Periot, O., Dilharreguy, B., Hiba, B., Bordessoules, M., Pérès, K., Amieva, H., Dartigues, J., Michèle Allard, A., & Catheline, G. (2013) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2013.00084 · Cited by 43
Anomalous White Matter Structure and the Effect of Age in Down Syndrome Patients
Fenoll, R., Pujol, J., Esteba‐Castillo, S., de Sola, S., Ribas‐Vidal, N., García‐Alba, J., Sánchez‐Benavides, G., Martínez‐Vilavella, G., Deus, J., Dierssen, M., et al. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-161112 · Cited by 43
Fitzgerald, J., Leemans, A., Kehoe, E. G., O’Hanlon, E., Gallagher, L., & McGrath, J. (2017) · European Journal of Neuroscience · doi:10.1111/ejn.13655 · Cited by 42
“…a voxel with fi bres crossing at right angles will be lower than the FA measured in a single fi bre population, and if one of these two crossing fi bres breaks down as a result of some pathological process, the FA will appear to increase in this region (Douaud et al. , 2011; Jeurissen et al. , 2013).”
Cavedo, E., Lista, S., Rojkova, K., Chiesa, P. A., Houot, M., Brueggen, K., Blautzik, J., Bokde, A. L. W., Dubois, B., Barkhof, F., et al. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.05.048 · Cited by 40
“between the corticospinal tract and the superior longitudinal fasciculus (Douaud et al., 2011) as previously reported also in diseased tissue (Amlien and Fjell, 2014).”
BackgroundLiu, T.-T., Gao, F.-S., Zheng, W., You, Y., Zhao, Z.-Y., Lv, Y., Chen, W., Zhang, H.-X., Ji, C., & Wu, D. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.118465 · Cited by 37
Yeung, M. K.-C., Chau, A. K.-Y., Chiu, J. Y.-C., Shek, J. T.-L., Leung, J. P.-Y., & Wong, T. C.-H. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101675 · Cited by 40
Hikishima, K., Ando, K., Yano, R., Kawai, K., Komaki, Y., Inoue, T., Itoh, T., Yamada, M., Momoshima, S., Okano, H. J., et al. (2015) · Radiology · doi:10.1148/radiol.14140601 · Cited by 41
Hippocampal Disconnection in Early Alzheimer's Disease: A 7 Tesla MRI Study
Wisse, L. E. M., Reijmer, Y. D., ter Telgte, A., Kuijf, H. J., Leemans, A., Luijten, P. R., Koek, H. L., Geerlings, M. I., Biessels, G. J., & on behalf of the Utrecht Vascular Cognitive Impairment (VCI) Study Group (2015) · Journal of Alzheimer s Disease · doi:10.3233/jad-142994 · Cited by 40
“Another limitation of our study is the possible effect of partial volume errors [6, 52, 53] and head motion [54] on the diffusion imaging parameters, in particular for small bundles such as the fornix, as well as the confounding effect of crossing fibers [55].”
Li, W., Muftuler, L. T., Chen, G., Ward, B. D., Budde, M. D., Jones, J. L., Franczak, M. B., Antuono, P., Li, S., & Goveas, J. S. (2013) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2013.12.016 · Cited by 40
“DA increases may be dependent on the microglial activation and clearance of axonal fragments, as well as degeneration affecting only one tract in areas with crossing fibers [42, 43].”
BackgroundBergamino, M., Kuplicki, R., Victor, T. A., Cha, Y., & Paulus, M. P. (2017) · Human Brain Mapping · doi:10.1002/hbm.23694 · Cited by 40
“Moreover, other investigators have proposed that increased FA in this tract can be connected to decreased FA in SLF [Douaud et al., 2011].”
BackgroundLoss and dispersion of superficial white matter in Alzheimer’s disease: a diffusion MRI study
Veale, T. D., Malone, I. B., Poole, T., Parker, T. D., Slattery, C. F., Paterson, R. W., Foulkes, A., Thomas, D. L., Schott, J. M., Zhang, H. G., et al. (2021) · Brain Communications · doi:10.1093/braincomms/fcab272 · Cited by 39
“61 However, with no corresponding NDI or ODI changes in these regions that met our FDR-corrected threshold for multiple comparisons, the specific microstructural changes driving DTI here are unclear.”
Nagarajan, I., & Priya, G. G. L. (2025) · Frontiers in Computer Science · doi:10.3389/fcomp.2024.1404494 · Cited by 47
de Luis-Garcı́a, R., Piñol, G. C., Roncero, C. Í., Argibay-Quiñones, D., Barrio-Arranz, G., Aja‐Fernández, S., & Alberola‐López, C. (2014) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2014.10.014 · Cited by 39
“LM is commonly employed in tractography algorithms, whereas TM has been employed in different studies on WM alterations (Douaud et al., 2011).”
MethodProgression of Microstructural Damage in Spinocerebellar Ataxia Type 2: A Longitudinal DTI Study
Mascalchi, M., Toschi, N., Giannelli, M., Ginestroni, A., Nave, R. D., Nicolai, E., Bianchi, A., Tessa, C., Salvatore, E., Aiello, M., et al. (2015) · American Journal of Neuroradiology · doi:10.3174/ajnr.a4343 · Cited by 40
“the potential use of the MO as an additional valuable and sensitive descriptor of microstructural changes.(41) We submit the following”
BackgroundMethodInfluentialHandiru, V. S., Alivar, A., Hoxha, A., Saleh, S., Suviseshamuthu, E. S., Yue, G. H., & Allexandre, D. (2021) · Human Brain Mapping · doi:10.1002/hbm.25554 · Cited by 40
“Furthermore, reduced MA would signify more disc-like, less cigar-like shape water diffusion, that is, 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.”
BackgroundSchäfer, A., Chaggar, P., Thompson, T., Goriely, A., Ellen Kuhl, A., & Initiative, F. T. A. D. N. (2021) · Brain Multiphysics · doi:10.1016/j.brain.2021.100039 · Cited by 44
Kato, S., Hagiwara, A., Yokoyama, K., Andica, C., Tomizawa, Y., Hoshino, Y., Uchida, W., Nishimura, Y., Fujita, S., Kamagata, K., et al. (2022) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2022.120205 · Cited by 39
“However, higher FA was reported in the centrum semiovale of Alzheimer's disease patients [52] and in the subcortical gray matter of Huntington's disease patients [53], suggesting this was due to a selective sparing (or selective degeneration) of certain fiber populations (i.”
Nishioka, C., Initiative, A. D. N., Poh, C., & Sun, S. (2015) · Journal of Alzheimer s Disease · doi:10.3233/jad-141239 · Cited by 40
Longitudinal diffusion tensor imaging in dementia with Lewy bodies and Alzheimer's disease
Firbank, M., Watson, R., Mak, E., Aribisala, B. S., Barber, R., Colloby, S. J., He, J., Blamire, A. M., & O'Brien, J. T. (2016) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2016.01.003 · Cited by 40
“[15, 18] We saw a relationship between change in FA and atrophy in only the control group.”
BackgroundMcAdams, R. M., Fleiss, B., Traudt, C. M., Schwendimann, L., Snyder, J. M., Haynes, R. L., Natarajan, N., Gressèns, P., & Juul, S. E. (2017) · Developmental Neuroscience · doi:10.1159/000470903 · Cited by 38
Rimol, L. M., Botellero, V. L., Bjuland, K. J., Løhaugen, G. C. C., Lydersen, S., Evensen, K. A. I., Brubakk, A., Eikenes, L., Indredavik, M. S., Martinussen, M., et al. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.11.050 · Cited by 38
“The interpretation of increased FA is not straightforward in a crossing fiber region (Douaud et al., 2011; Jones, 2010), but it could occur as a result of selective disruption to one of the fiber populations present (Tuch et al.”
The neurobiology of Alzheimer disease defined by neuroimaging
Masdeu, J. C., Kreisl, W. C., & Berman, K. F. (2012) · Current Opinion in Neurology · doi:10.1097/wco.0b013e3283557b36 · Cited by 39
Hirsiger, S., Koppelmans, V., Mérillat, S., Erdin, C., Narkhede, A., Brickman, A. M., & Jäncke, L. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00373 · Cited by 38
Lin, S.-Y., Lin, C., Hsieh, T.-J., Lin, C.-F., Chen, S.-H., Chao, Y., Chen, Y., Hsu, C.-C., & Kuo, L. (2019) · NeuroImage Clinical · doi:10.1016/j.nicl.2019.101680 · Cited by 37
“Fiber tracking with diffusion MRI can also be used to characterize the connective patterns of white matter (WM) tracts and has been widely used in AD research (Douaud et al., 2011; Kantarci et al., 2017; Nir et al., 2013).”
MethodHodgetts, C. J., Shine, J. P., Williams, H., Postans, M., Sims, R., Williams, J. H., Lawrence, A. D., & Graham, K. S. (2018) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2018.08.026 · Cited by 40
Distinct Types of White Matter Changes Are Observed after Anterior Temporal Lobectomy in Epilepsy
Pustina, D., Doucet, G. E., Evans, J. J., Sharan, A. D., Sperling, M. R., Skidmore, C. T., & Tracy, J. I. (2014) · PLoS ONE · doi:10.1371/journal.pone.0104211 · Cited by 37
“For example, it is not clear whether the limitations affecting parallel and perpendicular diffusivities in areas with crossing fibers [71], affect MO as well, a limitation that would alter its biological significance as a measure of crossing fibers [38,39].”
BackgroundMethodImaging Epigenetics in Alzheimer’s Disease
Lista, S., Garaci, F. G., Toschi, N., & Hampel, H. J. (2013) · Current Pharmaceutical Design · doi:10.2174/13816128113199990370 · Cited by 36
Mode of Anisotropy Reveals Global Diffusion Alterations in Attention-Deficit/Hyperactivity Disorder
Yoncheva, Y. N., Somandepalli, K., Reiss, P. T., Kelly, C. A. M., Martino, A. D., Lazar, M., Zhou, J. H., Milham, M. P., & Castellanos, F. X. (2015) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2015.11.011 · Cited by 38
White matter change with apathy and impulsivity in frontotemporal lobar degeneration syndromes
Lansdall, C. J., Coyle-Gilchrist, I. T. S., Jones, P. S., Rodríguez, P. V., Wilcox, A., Wehmann, E., Dick, K. M., Robbins, T. W., & Rowe, J. B. (2018) · Neurology · doi:10.1212/wnl.0000000000005175 · Cited by 40
“The warped FA images were averaged to produce a study-specific FA template.(17) Registration was repeated for all participants using this study-specific FA template as target, bringing all participants into the same anatomical space.”
MethodDiagnosis and prognosis of Alzheimer's disease using brain morphometry and white matter connectomes
Wang, Y., Xu, C., Park, J. H., Lee, S., Stern, Y., Yoo, S., Kim, J. H., Kim, H. S., Cha, J., & Initiative, T. A. D. N. (2019) · NeuroImage Clinical · doi:10.1016/j.nicl.2019.101859 · Cited by 40
Lin, A., Laird, A. R., Fox, P. T., & Gao, J. (2011) · Neurology Research International · doi:10.1155/2012/907409 · Cited by 36
“AD patients, similar to aMCI patients (but more severe), have shown significant increase in diffusion atrophy in the region of crossing fibers in the centrum semiovale (Figure 6; [34]), They have further shown regionally specific shape abnormalities and reduction in fractional anisotropy (FA) in the corpus callosum, a…”
BackgroundResultNir, T. M., Jahanshad, N., Villalon‐Reina, J. E., Isaev, D., Zavaliangos‐Petropulu, A., Zhan, L., Leow, A. D., Jack, C. R., Weiner, M. W., Thompson, P. M., et al. (2017) · Magnetic Resonance in Medicine · doi:10.1002/mrm.26623 · Cited by 34
“However, relative increases in FA have been reported in FA studies of AD, which may reflect a selective sparing or selective degeneration of one of the pathways in a region with crossing fibers (48).”
BackgroundWhite matter and nigral alterations in multiple system atrophy-parkinsonian type
Ogawa, T., Hatano, T., Kamagata, K., Andica, C., Takeshige‐Amano, H., Uchida, W., Kamiyama, D., Shimo, Y., Oyama, G., Umemura, A., et al. (2021) · npj Parkinson s Disease · doi:10.1038/s41531-021-00236-0 · Cited by 35
Surova, Y., Szczepankiewicz, F., Lätt, J., Nilsson, M., Eriksson, B., Leemans, A., Hansson, O., van Westen, D., & Nilsson, C. F. (2013) · PLoS ONE · doi:10.1371/journal.pone.0066022 · Cited by 32
“Notwithstanding the low specificity in assessing the cause of the observed diffusion abnormalities [72], DTI may still exhibit a high sensitivity, which has shown to be useful in several applications [73–74].”
McGrath, J., Johnson, K. A., O’Hanlon, E., Garavan, H., Gallagher, L., & Leemans, A. (2013) · Autism Research · doi:10.1002/aur.1290 · Cited by 34
Rasero, J., Alonso-Montes, C., Diez, I. P., Olabarrieta‐Landa, L., Remaki, L., Escudero, I., Goñi, B. M., Bonifazi, P., Fernández, M., Arango‐Lasprilla, J. C., et al. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00215 · Cited by 32
“Taking into consideration previous work (Khedher et al. 2015, Douaud et al. 2011, Bosch et al. 2012, Liu et al. 2013, Acosta-Cabronero et al. 2012, Preti et al. 2012), the present study focus on the variations of brain networks across AD progression at a group level.”
Kamiya, K., Kamagata, K., Ogaki, K., Hatano, T., Ogawa, T., Takeshige‐Amano, H., Murata, S., Andica, C., Murata, K., Feiweier, T., et al. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.584510 · Cited by 30
Εvangelou, Ε., Suzuki, H., Bai, W., Pazoki, R., Gao, H., Matthews, P. M., & Elliott, P. (2021) · eLife · doi:10.7554/elife.65325 · Cited by 31
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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