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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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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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BackgroundMethodThe basis of anisotropic water diffusion in the nervous system—A technical review.
Beaulieu, C. (2002) · NMR in Biomedicine · doi:10.1002/nbm.782 · Cited by 4,628
Gauthier, S. G., Reisberg, ., Zaudig, M., Petersen, R. C., Ritchie, K. A., Broich, K., Belleville, S., Brodaty, H., Bennett, D. A., Chertkow, H. M., et al. (2006) · The Lancet · doi:10.1016/s0140-6736(06)68542-5 · Cited by 4,094
Probabilistic diffusion tractography with multiple fibre orientations: What can we gain?
Behrens, T. E. J., Berg, H. J., Jbabdi, S., Rushworth, M. F. S., & Woolrich, M. W. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2006.09.018 · Cited by 3,471 · cited 5×
“To answer some specific questions that arose in the course of this clinical study, we came to use for the first time in a degenerative disorder a recently developed tensor index, the “mode” of anisotropy (Ennis and Kindlmann, 2006) and a new feature of probabilistic tractography (Behrens et al., 2007).”
BackgroundMethodInfluentialAlzheimer's disease: cell-specific pathology isolates the hippocampal formation.
Hyman, B. T., Van Hoesen, G. W., Damasio, A. R., & Barnes, C. L. (1984) · Science · doi:10.1126/science.6474172 · Cited by 2,268
Vitamin E and Donepezil for the Treatment of Mild Cognitive Impairment
Petersen, R. C., Thomas, R. G., Grundman, M., Bennett, D., Doody, R., Ferris, S., Galasko, D., Jin, S., Kaye, J., Levey, A., et al. (2005) · New England Journal of Medicine · doi:10.1056/nejmoa050151 · Cited by 1,844 · cited 2×
“…Ganguli, 2006), one MCI patient made a transition to dementia with Lewy bodies and 7 MCI patients made the transition to AD, in good accordance with a rate of conversion to AD of ~ 10–16% observed per year in other studies (Grundman et al., 2004; Petersen et al., 2005; Gauthier et al., 2006).”
ResultSong, S.-K., Sun, S.-W., Ju, W.-K., Lin, S.-J., Cross, A. H., & Neufeld, A. H. (2003) · NeuroImage · doi:10.1016/j.neuroimage.2003.07.005 · Cited by 1,738 · cited 2×
“As mentioned by the authors of the former study, this result seem indeed in opposition with what is expected from animal models and human corpus callosotomy demonstrating that axonal pathology or transection should result in a decrease in axial diffusivity (Song et al., 2003; Concha et al., 2006 ).”
ResultPrinciples of Frontal Lobe Function
Stuss, D. T. (2002) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195134971.001.0001 · Cited by 1,731
Microstructural maturation of the human brain from childhood to adulthood
Lebel, C., Walker, L., Leemans, A., Phillips, L., & Beaulieu, C. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2007.12.053 · Cited by 1,398 · cited 1×
“First, reduced FA is generally interpreted to reflect a decrease in the organisation of the white matter caused by various microstructural processes such as demyelination, axonal degradation or gliosis (Beaulieu, 2002; Concha et al., 2006; Lebel et al., 2008; Assaf, 2008).”
BackgroundDickerson, B. C., Bakkour, A., Salat, D. H., Feczko, E., Pacheco, J., Greve, D. N., Grodstein, F., Wright, C. I., Blacker, D., Rosas, H. D., et al. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhn113 · Cited by 1,153 · cited 2×
“, 2009), is likely reflected by the clinical preservation of the motor functions until later stages of the disease (95% of the AD patients included in this study had mild AD) and is consistent with the preservation of the sensorimotor cortex (Karas et al., 2004; Chetelat et al., 2008; Dickerson et al., 2009).”
ResultMakris, N., Kennedy, D. N., McInerney, S., Sorensen, A. G., Wang, R., Caviness, V. S., & Pandya, D. N. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhh186 · Cited by 1,146 · cited 1×
“The last tract we found impaired using all indices was the SLF, mainly in the section II of this tract, which extends from the angular gyrus to the caudal-lateral prefrontal regions (Makris et al., 2005).”
MethodGrundman, M. (2004) · Archives of Neurology · doi:10.1001/archneur.61.1.59 · Cited by 972 · cited 2×
“…Ganguli, 2006), one MCI patient made a transition to dementia with Lewy bodies and 7 MCI patients made the transition to AD, in good accordance with a rate of conversion to AD of ~ 10–16% observed per year in other studies (Grundman et al., 2004; Petersen et al., 2005; Gauthier et al., 2006).”
ResultDiffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers
Wedeen, V. J., Wang, R., Schmahmann, J. D., Benner, T., Tseng, W. I., Dai, G., Pandya, D. Ν., Hagmann, P., D'Arceuil, H. E., & de Crespigny, A. J. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.03.036 · Cited by 941 · cited 7×
“Tractography was then performed in standard space from every voxel of the same seed ROI for all subjects to trace two different pathways: the association fibres and the projection fibres running through this ROI (Wedeen et al., 2008).”
BackgroundMethodInfluentialWater diffusion changes in wallerian degeneration and their dependence on white matter architecture
Pierpaoli, C., Barnett, A., Pajevic, S., Chen, R., Penix, L., Virta, A., & Basser, P. (2001) · NeuroImage · doi:10.1006/nimg.2001.0765 · Cited by 938 · cited 1×
“By contrast, the unusual increase of FA – in the context of a neurodegenerative disorder – is likely related to a selective sparing (or selective degeneration) of one of the pathways in a region of crossing fibres (Pierpaoli et al., 2001; Douaud et al., 2009).”
BackgroundDiffusion tensor imaging and aging
Sullivan, E. V., & Pfefferbaum, A. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2006.06.002 · Cited by 649 · cited 2×
“Increases in MD have often been reported in studies on age- or disease-related neurodegeneration (reviews in Moseley, 2002; Bozzali and Cherubini, 2007; Sullivan and Pfefferbaum, 2006).”
BackgroundHead, D. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh003 · Cited by 645 · cited 2×
“, 2007), there has been conflicting evidence about whether the genu (Head et al., 2004; Xie et al., 2006) or the splenium (Rose et al.”
BackgroundGlobal and local gray matter loss in mild cognitive impairment and Alzheimer's disease
Karas, G. B., Scheltens, P., Rombouts, S. A. R. B., Visser, P. J., van Schijndel, R. A., Fox, N. C., & Barkhof, F. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.07.006 · Cited by 613 · cited 4×
“, 2009), is likely reflected by the clinical preservation of the motor functions until later stages of the disease (95% of the AD patients included in this study had mild AD) and is consistent with the preservation of the sensorimotor cortex (Karas et al., 2004; Chetelat et al., 2008; Dickerson et al., 2009).”
BackgroundResultInfluentialBozzali, M. (2002) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.72.6.742 · Cited by 568 · cited 4×
“The relative sparing of the motor pathways in AD, evidenced so far by a lack of significant FA changes (Rose et al., 2000; Bozzali et al., 2002; Takahashi et al., 2002; Kiuchi et al., 2009), is likely reflected by the clinical preservation of the motor functions until later stages of the disease (95% of the AD patient…”
BackgroundMethodResultInfluentialPrinciples of frontal lobe function
Jellinger, K. A. (2003) · European Journal of Neurology · doi:10.1046/j.1468-1331.2003.00507_2.x · Cited by 562
Diffusion tensor imaging of cingulum fibers in mild cognitive impairment and Alzheimer disease
Zhang, Y., Schuff, N. W., Jahng, G., Bayne, W., Mori, S., Schad, L. R., Mueller, S. G., Du, A., Kramer, J. H., Yaffe, K. S., et al. (2007) · Neurology · doi:10.1212/01.wnl.0000250326.77323.01 · Cited by 513
White matter changes in mild cognitive impairment and AD: a diffusion tensor imaging study
Medina, D., deToledo-Morrell, L., Urresta, F., Gabrieli, J. D. E., Moseley, M., Fleischman, D., Bennett, D. A., Leurgans, S., Turner, D. A., & Stebbins, G. T. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.03.026 · Cited by 492 · cited 3×
“Particularly, to our knowledge only three such studies examined healthy elderly, MCI and AD populations together, with quite limited population samples (Medina et al., 2006; Serra et al., 2010; Liu et al., 2009).”
BackgroundRose, S. (2000) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.69.4.528 · Cited by 465 · cited 5×
“Decrease of FA and increase of MD in the SLF are consistent with previous findings in AD (Rose et al., 2000; Takahashi et al., 2002; Parente et al., 2008).”
BackgroundResultInfluentialAbsolute diffusivities define the landscape of white matter degeneration in Alzheimer’s disease
Acosta-Cabronero, J., Williams, G. B., Pengas, G., & Nestor, P. J. (2010) · Brain · doi:10.1093/brain/awp257 · Cited by 393
Hua, X., Leow, A., Parikshak, N., Lee, S., Chiang, M.-C., Toga, A. W., Jack, C. R., Weiner, M. W., & Thompson, P. M. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.07.013 · Cited by 372 · cited 2×
“…MCI patients compared with healthy controls is mostly confined to the medial temporal lobe and posterior cingulate/precuneus (Whitwell et al., 2008; Hua et al., 2008; Choo et al., 2010), the impairment of the SLF witnessed in crossing fibre regions using the mode of anisotropy might be the…”
Tuch, D. S., Salat, D. H., Wisco, J. J., Zaleta, A. K., Hevelone, N. D., & Rosas, H. D. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407259102 · Cited by 364 · cited 2×
“Finally, we believe that the methods used in this study have general applicability for other degenerative disorders and that, beyond the clinical sphere, these methods could contribute to a better understanding and quantification of subtle effects witnessed in normal processes such as visuospatial attention (Tuch et a…”
MethodMRI patterns of atrophy associated with progression to AD in amnestic mild cognitive impairment
Whitwell, J. L., Shiung, M. M., Przybelski, S. A., Weigand, S. D., Knopman, D. S., Boeve, B. F., Petersen, R. C., & Jack, C. R. (2008) · Neurology · doi:10.1212/01.wnl.0000280575.77437.a2 · Cited by 357 · cited 2×
“…grey matter loss in MCI patients compared with healthy controls is mostly confined to the medial temporal lobe and posterior cingulate/precuneus (Whitwell et al., 2008; Hua et al., 2008; Choo et al., 2010), the impairment of the SLF witnessed in crossing fibre regions using the mode of…”
BackgroundDirect voxel-based comparison between grey matter hypometabolism and atrophy in Alzheimer's disease
Chételat, G., Desgranges, B., Landeau, B., Mézenge, F., Poline, J.-B., Sayette, V. D. L., Viader, F., Eustache, F., & Baron, J. (2007) · Brain · doi:10.1093/brain/awm288 · Cited by 349 · cited 2×
“, 2009), is likely reflected by the clinical preservation of the motor functions until later stages of the disease (95% of the AD patients included in this study had mild AD) and is consistent with the preservation of the sensorimotor cortex (Karas et al., 2004; Chetelat et al., 2008; Dickerson et al., 2009).”
ResultStricker, N. H., Schweinsburg, B. C., Delano‐Wood, L., Wierenga, C. E., Bangen, K. J., Haaland, K. Y., Frank, L. R., Salmon, D. P., & Bondi, M. W. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.11.027 · Cited by 318 · cited 2×
“…(reviews in Bozzali and Cherubini, 2007; Chua et al., 2008; Hess, 2009), there have been few whole-brain voxel-wise studies in which no a priori hypothesis was made regarding anatomical localisation of white matter abnormalities (e.g. Rose et al., 2006; Teipel et al., 2007; Stricker et al., 2009).”
BackgroundDiffusion tensor imaging and aging—A review.
Moseley, M. (2002) · NMR in Biomedicine · doi:10.1002/nbm.785 · Cited by 302 · cited 1×
“Increases in MD have often been reported in studies on age-or disease-related neurodegeneration (reviews in Moseley, 2002; Bozzali and Cherubini, 2007; Sullivan and Pfefferbaum, 2006 ).”
BackgroundFellgiebel, A., Wille, P., Müller, M. J., Winterer, G., Scheurich, A., Vucurevic, G., Schmidt, L. G., & Stoeter, P. (2004) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000077817 · Cited by 298 · cited 2×
“On the other hand, while a reduced FA and/ or an increased MD in the corpus callosum is one of the most consistent findings in AD (Fellgiebel et al., 2004; Stahl et al., 2007), there has been conflicting evidence about whether the genu (Head et al., 2004; Xie et al., 2006) or the splenium (Rose et…”
BackgroundConcha, L., Gross, D. W., Wheatley, B. M., & Beaulieu, C. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.04.187 · Cited by 293 · cited 3×
“As mentioned by the authors of the former study, this result seem indeed in opposition with what is expected from animal models and human corpus callosotomy demonstrating that axonal pathology or transection should result in a decrease in axial diffusivity (Song et al., 2003; Concha et al., 2006 ).”
BackgroundResultWhite matter pathology isolates the hippocampal formation in Alzheimer's disease
Salat, D. H., Tuch, D. S., van der Kouwe, A. J. W., Greve, D. N., Pappu, V., Lee, S. Y., Hevelone, N. D., Zaleta, A. K., Growdon, J. H., Corkin, S., et al. (2010) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2008.03.013 · Cited by 279 · cited 1×
“…the cingulum bundle and the uncinate fasciculus, consistent with previous studies showing reduced FA and increased MD in the cingulum bundle (Bozzali et al., 2002; Fellgiebel et al., 2005; Zhang et al., 2007; Salat et al., 2010) or the uncinate fasciculus (Taoka et al., 2006; Kiuchi et al., 2009).”
Orthogonal tensor invariants and the analysis of diffusion tensor magnetic resonance images
Ennis, D. B., & Kindlmann, G. (2006) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20741 · Cited by 276 · cited 5×
“…whole-brain diffusion differences between MCI patients and healthy subjects, the only region where we found significant abnormalities was a region of crossing fibres in the centrum semiovale, showing an increase of mode of anisotropy, a recently developed tensor index (Ennis and Kindlmann, 2006).”
BackgroundMethodInfluentialSelf-citationDiffusion tensor imaging in mild cognitive impairment and Alzheimerʼs disease: a review
Chua, T. C., Wen, W., Slavin, M. J., & Sachdev, P. S. (2008) · Current Opinion in Neurology · doi:10.1097/wco.0b013e3282f4594b · Cited by 273 · cited 5×
“As expected from the literature (reviews in Chua et al., 2008; Hess, 2009), all indices converged to demonstrate white matter microstructural changes in the cingulum bundle, uncinate fasciculus, corpus callosum, anterior commissure and SLF in patients with AD.”
BackgroundResultInfluentialFellgiebel, A., Müller, M. J., Wille, P. R., Dellani, P. R., Scheurich, A., Schmidt, L., & Stoeter, P. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2004.11.006 · Cited by 266 · cited 2×
“…the cingulum bundle and the uncinate fasciculus, consistent with previous studies showing reduced FA and increased MD in the cingulum bundle (Bozzali et al., 2002; Fellgiebel et al., 2005; Zhang et al., 2007; Salat et al., 2010) or the uncinate fasciculus (Taoka et al., 2006; Kiuchi et al., 2009).”
MethodAssociation Pathways of the Prefrontal Cortex and Functional Observations
Petrides, M., & Pandya, D. Ν. (2002) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195134971.003.0003 · Cited by 260 · cited 1×
“Damage to the SLF II is known to result in disorders of spatial working memory (Preuss and Goldman-Rakic, 1989; Petrides and Pandya, 2002).”
BackgroundPreuss, T. M., & Goldman, P. S. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902820210 · Cited by 247 · cited 1×
“Damage to the SLF II is known to result in disorders of spatial working memory (Preuss and Goldman-Rakic, 1989; Petrides and Pandya, 2002).”
BackgroundEarly Diagnosis of Alzheimers Disease: Is MCI Too Late?
Petersen, R. C. (2009) · Current Alzheimer Research · doi:10.2174/156720509788929237 · Cited by 239 · cited 2×
“On the other hand, mild cognitive impairment (MCI) is an intermediate clinical state between the cognitive changes of aging and the earliest clinical manifestations of AD (Petersen, 2009), with more than half of the MCI population progressing todementiawithin 5 years (Gauthier et al.”
BackgroundLiu, Y., Spulber, G., Lehtimäki, K. K., Könönen, M., Hallikainen, I., Gröhn, H., Kivipelto, M., Hallikainen, M., Vanninen, R., & Soininen, H. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2009.10.006 · Cited by 236 · cited 2×
“Particularly, to our knowledge only three such studies examined healthy elderly, MCI and AD populations together, with quite limited population samples (Medina et al., 2006; Serra et al., 2010; Liu et al., 2009).”
BackgroundTakahashi, S., Yonezawa, H., Takahashi, J., Kudo, M., Inoue, T., & Tohgi, H. (2002) · Neuroscience Letters · doi:10.1016/s0304-3940(02)00914-x · Cited by 225 · cited 5×
“Decrease of FA and increase of MD in the SLF are consistent with previous findings in AD (Rose et al., 2000; Takahashi et al., 2002; Parente et al., 2008).”
BackgroundResultInfluentialStahl, R., Dietrich, O., Teipel, S. J., Hampel, H. J., Reiser, M. F., & Schoenberg, S. O. (2007) · Radiology · doi:10.1148/radiol.2432051714 · Cited by 215 · cited 2×
“…other hand, while a reduced FA and/ or an increased MD in the corpus callosum is one of the most consistent findings in AD (Fellgiebel et al., 2004; Stahl et al., 2007), there has been conflicting evidence about whether the genu (Head et al., 2004; Xie et al., 2006) or the splenium (Rose et al.,…”
BackgroundChoo, I. H., Lee, D. Y., Oh, J. S., Lee, J. S., Lee, D. S., Song, I. C., Youn, J. C., Kim, S. G., Kim, K. W., Jhoo, J. H., et al. (2010) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2008.06.015 · Cited by 211 · cited 2×
“As it would seem that grey matter loss in MCI patients compared with healthy controls is mostly confined to the medial temporal lobe and posterior cingulate/precuneus (Whitwell et al., 2008; Hua et al., 2008; Choo et al., 2010), the impairment of the SLF witnessed in crossing fibre regions using the mode of anisotropy…”
BackgroundVoxel-based detection of white matter abnormalities in mild Alzheimer disease
Xie, S., Xiao, J., Gong, G., Zang, Y., Wang, Y., Wu, H., & Jiang, X. X. (2006) · Neurology · doi:10.1212/01.wnl.0000219625.77625.aa · Cited by 208 · cited 2×
“…consistent findings in AD (Fellgiebel et al., 2004; Stahl et al., 2007), there has been conflicting evidence about whether the genu (Head et al., 2004; Xie et al., 2006) or the splenium (Rose et al., 2000; Takahashi et al., 2002; Medina et al., 2006) shows the greatest neuropathological changes.”
BackgroundIn vivo evidence for the selective subcortical degeneration in Huntington's disease
Douaud, G., Behrens, T. E. J., Poupon, C., Cointepas, Y., Jbabdi, S., Gaura-Schmidt, V., Golestani, N., Krystkowiak, P. C., Verny, C., Damier, P., et al. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.03.044 · Cited by 203 · cited 3×
“We should first be able to confirm this theory with a colocalised increase of FA, increase that has been previously shown to characterise a selective degeneration in crossing fibre region (Douaud et al., 2009).”
BackgroundResultRose, S. (2006) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.2005.074336 · Cited by 189 · cited 1×
“…(reviews in Bozzali and Cherubini, 2007; Chua et al., 2008; Hess, 2009), there have been few whole-brain voxel-wise studies in which no a priori hypothesis was made regarding anatomical localisation of white matter abnormalities (e.g. Rose et al., 2006; Teipel et al., 2007; Stricker et al., 2009).”
BackgroundMultivariate network analysis of fiber tract integrity in Alzheimer’s disease
Teipel, S. J., Stahl, R., Dietrich, O., Schoenberg, S. O., Perneczky, R., Bokde, A. L. W., Reiser, M. F., Möller, H., & Hampel, H. J. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.07.047 · Cited by 169 · cited 2×
“…(reviews in Bozzali and Cherubini, 2007; Chua et al., 2008; Hess, 2009), there have been few whole-brain voxel-wise studies in which no a priori hypothesis was made regarding anatomical localisation of white matter abnormalities (e.g. Rose et al., 2006; Teipel et al., 2007; Stricker et al., 2009).”
BackgroundCedazo-Mínguez, Á., & Winblad, B. G. (2009) · Experimental Gerontology · doi:10.1016/j.exger.2009.09.008 · Cited by 159
Disrupted myelin and axon loss in the anterior commissure of the aged rhesus monkey
Sandell, J. H., & Peters, A. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10859 · Cited by 158 · cited 1×
“Interestingly, electron microscopy in aging rhesus monkeys has demonstrated age-related alteration and degeneration of the myelinated fibres in this structure (Sandell and Peters, 2003).”
BackgroundGrey and white matter changes at different stages of Alzheimer’s disease
Serra, L., Cercignani, M., Lenzi, D., Perri, R., Fadda, L., Caltagirone, C., Macaluso, E., & Bozzali, M. (2010) · Journal of Alzheimer's Disease · doi:10.3233/jad-2010-1223 · Cited by 149 · cited 5×
“Particularly, to our knowledge only three such studies examined healthy elderly, MCI and AD populations together, with quite limited population samples (Medina et al., 2006; Serra et al., 2010; Liu et al., 2009).”
BackgroundResultInfluentialTaoka, T., Iwasaki, S., Sakamoto, M., Nakagawa, H., Fukusumi, A., Myochin, K., Hirohashi, S., Hoshida, T., & Kichikawa, K. (2006) · PubMed Central · Cited by 127
Kiuchi, K., Morikawa, M., Taoka, T., Nagashima, T., Yamauchi, T., Makinodan, M., Norimoto, K., Hashimoto, K., Kosaka, J., Inoue, Y., et al. (2009) · Brain Research · doi:10.1016/j.brainres.2009.06.052 · Cited by 118 · cited 4×
“The relative sparing of the motor pathways in AD, evidenced so far by a lack of significant FA changes (Rose et al., 2000; Bozzali et al., 2002; Takahashi et al., 2002; Kiuchi et al., 2009), is likely reflected by the clinical preservation of the motor functions until later stages of the disease (95% of the AD patient…”
BackgroundMethodResultInfluentialSydykova, D., Stahl, R., Dietrich, O., Ewers, M., Reiser, M. F., Schoenberg, S. O., Möller, H. ‐., Hampel, H. J., & Teipel, S. J. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl136 · Cited by 84 · cited 1×
“Diffusion abnormalities in this tract are thought to be a manifestation of Wallerian degeneration in AD, as shown by correlations between the FA in the corpus callosum and the GM volume in various cortical regions only found in the AD patients (Sydykova et al., 2007).”
BackgroundDiffusion tensor MRI to investigate dementias: a brief review
Bozzali, M., & Cherubini, A. (2007) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2007.03.017 · Cited by 80 · cited 3×
“Increases in MD have often been reported in studies on age- or disease-related neurodegeneration (reviews in Moseley, 2002; Bozzali and Cherubini, 2007; Sullivan and Pfefferbaum, 2006).”
BackgroundParente, D., Gasparetto, E., da Cruz, L. C. H., Domingues, R. C., Baptista, A. C., Carvalho, A. C., & Domingues, R. (2008) · AJR. American journal of roentgenology · doi:10.2214/ajr.07.2617 · Cited by 75 · cited 1×
“Decrease of FA and increase of MD in the SLF are consistent with previous findings in AD (Rose et al., 2000; Takahashi et al., 2002; Parente et al., 2008).”
ResultCan we use diffusion MRI as a bio-marker of neurodegenerative processes?
Assaf, Y. (2008) · Bioessays · doi:10.1002/bies.20851 · Cited by 47 · cited 1×
“First, reduced FA is generally interpreted to reflect a decrease in the organisation of the white matter caused by various microstructural processes such as demyelination, axonal degradation or gliosis (Beaulieu, 2002; Concha et al., 2006; Lebel et al., 2008; Assaf, 2008).”
BackgroundMild Cognitive Impairment and the 7 Uses of Epidemiology
Ganguli, M. (2006) · Alzheimer Disease & Associated Disorders · doi:10.1097/00002093-200607001-00007 · Cited by 33 · cited 3×
“It would seem that for the clinically more heterogeneous population of MCI patients (compared with probable AD patients, Ganguli, 2006), considering a subject-specific balance or ratio between spared and affected tracts provides a more sensitive measure than just looking at the affected ones, as it…”
BackgroundResultInfluentialUpdate on Diffusion Tensor Imaging in Alzheimer's Disease
Hess, C. P. (2009) · Magnetic Resonance Imaging Clinics of North America · doi:10.1016/j.mric.2009.02.003 · Cited by 28 · cited 7×
“More than 35 million people will be suffering from dementia in 2010 (World Alzheimer report 2009, http://www.alz.co.uk/research/worldreport ) but a clinical diagnosis of Alzheimer's disease (AD) can only be made after development of disabling dementia (Cedazo-Monguez and Winblad, 2010; Hess, 2009).”
BackgroundResultInfluentialPhilippon, J. H., & Baldwin, M. (1971) · Acta Neurochirurgica · doi:10.1007/bf01401861 · Cited by 2 · cited 1×
“Another commissural pathway, the anterior commissure connecting temporal lobe, orbitofrontal cortex and amygdala (Philippon and Baldwin, 1971) showed the same diffusion changes (FA/MO decrease, and MD increase).”
Background
Cited by
Sorted by citations
Multimodal population brain imaging in the UK Biobank prospective epidemiological study
Miller, K. L., Alfaro-Almagro, F., Bangerter, N. K., Thomas, D. L., Yacoub, E., Xu, J., Bartsch, A. J., Jbabdi, S., Sotiropoulos, S. N., Andersson, J. L. R., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4393 · Cited by 2,020
“…exhibit the opposite, of FA increasing with aging, which may reflect degradation of secondary fibers or reduced fiber dispersion23; notably, none of the FA-based IDPs exhibit this significant positive correlation, demonstrating that averaging across tracts can sacrifice richness of information.”
SARS-CoV-2 is associated with changes in brain structure in UK Biobank
Douaud, G., Lee, S., Alfaro-Almagro, F., Arthofer, C., Wang, C., McCarthy, P., Lange, F., Andersson, J. L. R., Griffanti, L., Duff, E., et al. (2022) · Nature · doi:10.1038/s41586-022-04569-5 · Cited by 1,646
Jeurissen, B., Leemans, A., Tournier, J., Jones, D. K., & Sijbers, J. (2013) · Human Brain Mapping · doi:10.1002/hbm.22099 · Cited by 1,088
“In yet another study, increased diffusion anisotropy was measured in the centrum semiovale of patients with mild cognitive impairment and mild Alzheimer’s disease [Douaud et al., 2011].”
BackgroundDubois, J., Dehaene-Lambertz, G., Kulikova, S., Poupon, C., Hüppi, P. S., & Hertz-Pannier, L. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2013.12.044 · Cited by 851
“bundles follow different maturational calendars: when the first bundle gets myelinated, anisotropy first increases, but it subsequently decreases when the second crossing bundle gets mature (the reverse argument has been detailed for neurodegenerative disorders (Douaud et al., 2011)); at the same time, diffusivities a…”
BackgroundA hitchhiker's guide to diffusion tensor imaging
Soares, J. M., Marques, P., Alves, V., & Sousa, N. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00031 · Cited by 893
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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