White matter alterations in Parkinson's disease with normal cognition precede grey matter atrophy
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem
Grantová podpora
UL1 TR000114
NCATS NIH HHS - United States
UL1TR000114
NIH HHS - United States
PubMed
29304183
PubMed Central
PMC5755732
DOI
10.1371/journal.pone.0187939
PII: PONE-D-17-12041
Knihovny.cz E-zdroje
- MeSH
- atrofie MeSH
- bílá hmota diagnostické zobrazování patologie MeSH
- dospělí MeSH
- kognice MeSH
- lidé středního věku MeSH
- lidé MeSH
- magnetická rezonanční tomografie MeSH
- neuropsychologické testy MeSH
- neurozobrazování MeSH
- Parkinsonova nemoc diagnostické zobrazování patologie psychologie MeSH
- progrese nemoci MeSH
- šedá hmota diagnostické zobrazování patologie MeSH
- senioři MeSH
- studie případů a kontrol MeSH
- Check Tag
- dospělí MeSH
- lidé středního věku MeSH
- lidé MeSH
- mužské pohlaví MeSH
- senioři MeSH
- ženské pohlaví MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, N.I.H., Extramural MeSH
INTRODUCTION: While progressive MRI brain changes characterize advanced Parkinson's disease (PD), little has been discovered about structural alterations in the earliest phase of the disease, i.e. in patients with motor symptoms and with normal cognition. Our study aimed to detect grey matter (GM) and white matter (WM) changes in PD patients without cognitive impairment. METHODS: Twenty PD patients and twenty-one healthy controls (HC) were tested for attention, executive function, working memory, and visuospatial and language domains. High-resolution T1-weighted and 60 directional diffusion-weighted 3T MRI images were acquired. The cortical, deep GM and WM volumes and density, as well as the diffusion properties of WM, were calculated. Analyses were repeated on data flipped to the side of the disease origin. RESULTS: PD patients did not show any significant differences from HC in cognitive functioning or in brain volumes. Decreased GM intensity was found in the left superior parietal lobe in the right (p<0.02) and left (p<0.01) flipped data. The analysis of original, un-flipped data demonstrated elevated axial diffusivity (p<0.01) in the superior and anterior corona radiata, internal capsule, and external capsule in the left hemisphere of PD relative to HC, while higher mean and radial diffusivity were discovered in the right (p<0.02 and p<0.03, respectively) and left (p<0.02 and p<0.02, respectively) in the fronto-temporal WM utilizing flipped data. CONCLUSIONS: PD patients without cognitive impairment and GM atrophy demonstrated widespread alterations of WM microstructure. Thus, WM impairment in PD might be a sensitive sign preceding the neuronal loss in associated GM regions.
Central European Institute of Technology Masaryk University Neuroscience Centre Brno Czech Republic
Department of Neurology Albert Szent Györgyi Clinical Center University of Szeged Szeged Hungary
Department of Pediatrics University of Minnesota Minneapolis Minnesota United States of America
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Aarsland D, Bronnick K, Larsen JP, Tysnes OB, Alves G, Norwegian ParkWest Study G. Cognitive impairment in incident, untreated Parkinson disease: the Norwegian ParkWest study. Neurology. 2009;72(13):1121–6. doi: 10.1212/01.wnl.0000338632.00552.cb . PubMed DOI
Schrag A, Siddiqui UF, Anastasiou Z, Weintraub D, Schott JM. Clinical variables and biomarkers in prediction of cognitive impairment in patients with newly diagnosed Parkinson’s disease: a cohort study. The Lancet Neurology. 2016. doi: 10.1016/S1474-4422(16)30328-3 . PubMed DOI PMC
Chen L, Yu C, Zhang N, Liu J, Liu W. Cognitive impairment in patients with Parkinson’s disease: A 30-month follow-up study. Clinical Neurology and Neurosurgery. 2016;151:65–9. doi: 10.1016/j.clineuro.2016.09.021 . PubMed DOI
Mak E, Su L, Williams GB, O′Brien JT. Neuroimaging correlates of cognitive impairment and dementia in Parkinson’s disease. Parkinsonism & Related Disorders. 2015;21(8):862–70. doi: 10.1016/j.parkreldis.2015.05.013 . PubMed DOI
Melzer TR, Watts R, MacAskill MR, Pitcher TL, Livingston L, Keenan RJ, et al. White matter microstructure deteriorates across cognitive stages in Parkinson disease. Neurology. 2013;80(20):1841–9. doi: 10.1212/WNL.0b013e3182929f62 . PubMed DOI
Hattori T, Orimo S, Aoki S, Ito K, Abe O, Amano A, et al. Cognitive status correlates with white matter alteration in Parkinson’s disease. Human Brain Mapping. 2012;33(3):727–39. doi: 10.1002/hbm.21245 . PubMed DOI PMC
Auning E, Kjaervik VK, Selnes P, Aarsland D, Haram A, Bjornerud A, et al. White matter integrity and cognition in Parkinson’s disease: a cross-sectional study. BMJ open. 2014;4(1):e003976 doi: 10.1136/bmjopen-2013-003976 . PubMed DOI PMC
Sterling NW, Du G, Lewis MM, Swavely S, Kong L, Styner M, et al. Cortical gray and subcortical white matter associations in Parkinson’s disease. Neurobiology of Aging. 2016;49:100–8. doi: 10.1016/j.neurobiolaging.2016.09.015 . PubMed DOI PMC
Agosta F, Canu E, Stojkovic T, Pievani M, Tomic A, Sarro L, et al. The topography of brain damage at different stages of Parkinson’s disease. Human Brain Mapping. 2013;34(11):2798–807. doi: 10.1002/hbm.22101 . PubMed DOI PMC
Zhang J, Zhang YT, Hu WD, Li L, Liu GY, Bai YP. Gray matter atrophy in patients with Parkinson’s disease and those with mild cognitive impairment: a voxel-based morphometry study. International Journal of Clinical and Experimental Medicine. 2015;8(9):15383–92. . PubMed PMC
Chen FX, Kang DZ, Chen FY, Liu Y, Wu G, Li X, et al. Gray matter atrophy associated with mild cognitive impairment in Parkinson’s disease. Neuroscience Letters. 2016;617:160–5. doi: 10.1016/j.neulet.2015.12.055 . PubMed DOI
Schneider CB, Donix M, Linse K, Werner A, Fauser M, Klingelhoefer L, et al. Accelerated Age-Dependent Hippocampal Volume Loss in Parkinson Disease With Mild Cognitive Impairment. American Journal of Alzheimer’s Disease and Other Dementias. 2017:1533317517698794 doi: 10.1177/1533317517698794 . PubMed DOI PMC
Weintraub D, Doshi J, Koka D, Davatzikos C, Siderowf AD, Duda JE, et al. Neurodegeneration across stages of cognitive decline in Parkinson disease. Archives of Neurology. 2011;68(12):1562–8. doi: 10.1001/archneurol.2011.725 . PubMed DOI PMC
Lee JE, Park B, Song SK, Sohn YH, Park HJ, Lee PH. A comparison of gray and white matter density in patients with Parkinson’s disease dementia and dementia with Lewy bodies using voxel-based morphometry. Movement Disorders: Official Journal of the Movement Disorder Society. 2010;25(1):28–34. doi: 10.1002/mds.22858 . PubMed DOI
Agosta F, Pievani M, Sala S, Geroldi C, Galluzzi S, Frisoni GB, et al. White matter damage in Alzheimer disease and its relationship to gray matter atrophy. Radiology. 2011;258(3):853–63. doi: 10.1148/radiol.10101284 . PubMed DOI
Pierpaoli C, Barnett A, Pajevic S, Chen R, Penix LR, Virta A, et al. Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. NeuroImage. 2001;13(6 Pt 1):1174–85. doi: 10.1006/nimg.2001.0765 . PubMed DOI
Alexander AL, Hurley SA, Samsonov AA, Adluru N, Hosseinbor AP, Mossahebi P, et al. Characterization of cerebral white matter properties using quantitative magnetic resonance imaging stains. Brain Connectivity. 2011;1(6):423–46. doi: 10.1089/brain.2011.0071 . PubMed DOI PMC
Szabo N, Kincses ZT, Pardutz A, Toth E, Szok D, Csete G, et al. White matter disintegration in cluster headache. The Journal of Headache and Pain. 2013;14:64 doi: 10.1186/1129-2377-14-64 . PubMed DOI PMC
Kiraly A, Szabo N, Pardutz A, Toth E, Tajti J, Csete G, et al. Macro- and microstructural alterations of the subcortical structures in episodic cluster headache. Cephalalgia: an International Journal of Headache. 2017:333102417703762 doi: 10.1177/0333102417703762 . PubMed DOI
Koelkebeck K, Miyata J, Kubota M, Kohl W, Son S, Fukuyama H, et al. The contribution of cortical thickness and surface area to gray matter asymmetries in the healthy human brain. Human Brain Mapping. 2014;35(12):6011–22. doi: 10.1002/hbm.22601 . PubMed DOI PMC
Jenkinson M, Smith S. A global optimisation method for robust affine registration of brain images. Medical Image Analysis. 2001;5(2):143–56. . PubMed
Smith SM. Fast robust automated brain extraction. Human Brain Mapping. 2002;17(3):143–55. doi: 10.1002/hbm.10062 . PubMed DOI PMC
Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, et al. Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage. 2004;23 Suppl 1:S208–19. Epub 2004/10/27. doi: 10.1016/j.neuroimage.2004.07.051 . PubMed DOI
Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, et al. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. NeuroImage. 2006;31(4):1487–505. doi: 10.1016/j.neuroimage.2006.02.024 . PubMed DOI
Smith SM, Nichols TE. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage. 2009;44(1):83–98. doi: 10.1016/j.neuroimage.2008.03.061 . PubMed DOI
Smith SM, Zhang Y, Jenkinson M, Chen J, Matthews PM, Federico A, et al. Accurate, robust, and automated longitudinal and cross-sectional brain change analysis. NeuroImage. 2002;17(1):479–89. . PubMed
Zhang Y, Brady M, Smith S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Transactions on Medical Imaging. 2001;20(1):45–57. doi: 10.1109/42.906424 . PubMed DOI
Ashburner J, Friston KJ. Voxel-based morphometry—the methods. NeuroImage. 2000;11(6 Pt 1):805–21. doi: 10.1006/nimg.2000.0582 . PubMed DOI
Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage. 2002;17(2):825–41. . PubMed
Andersson JLR, Jenkinson M, Smith S. Non-linear optimisation FMRIB Technical Report. Oxford: 2007.
Patenaude B, Smith SM, Kennedy DN, Jenkinson M. A Bayesian model of shape and appearance for subcortical brain segmentation. NeuroImage. 2011;56(3):907–22. doi: 10.1016/j.neuroimage.2011.02.046 . PubMed DOI PMC
Claassen DO, McDonell KE, Donahue M, Rawal S, Wylie SA, Neimat JS, et al. Cortical asymmetry in Parkinson’s disease: early susceptibility of the left hemisphere. Brain and Behavior. 2016;6(12):e00573 doi: 10.1002/brb3.573 . PubMed DOI PMC
Caminiti SP, Presotto L, Baroncini D, Garibotto V, Moresco RM, Gianolli L, et al. Axonal damage and loss of connectivity in nigrostriatal and mesolimbic dopamine pathways in early Parkinson’s disease. NeuroImage Clinical. 2017;14:734–40. doi: 10.1016/j.nicl.2017.03.011 . PubMed DOI PMC
Rektorova I, Biundo R, Marecek R, Weis L, Aarsland D, Antonini A. Grey matter changes in cognitively impaired Parkinson’s disease patients. PloS One. 2014;9(1):e85595 doi: 10.1371/journal.pone.0085595 . PubMed DOI PMC
Vandenberghe R, Molenberghs P, Gillebert CR. Spatial attention deficits in humans: the critical role of superior compared to inferior parietal lesions. Neuropsychologia. 2012;50(6):1092–103. doi: 10.1016/j.neuropsychologia.2011.12.016 . PubMed DOI
Zhang K, Yu C, Zhang Y, Wu X, Zhu C, Chan P, et al. Voxel-based analysis of diffusion tensor indices in the brain in patients with Parkinson’s disease. European Journal of Radiology. 2011;77(2):269–73. doi: 10.1016/j.ejrad.2009.07.032 . PubMed DOI
Ibarretxe-Bilbao N, Junque C, Segura B, Baggio HC, Marti MJ, Valldeoriola F, et al. Progression of cortical thinning in early Parkinson’s disease. Movement Disorders: Official Journal of the Movement Disorder Society. 2012;27(14):1746–53. doi: 10.1002/mds.25240 . PubMed DOI
Filoteo JV, Reed JD, Litvan I, Harrington DL. Volumetric correlates of cognitive functioning in nondemented patients with Parkinson’s disease. Movement Disorders: Official Journal of the Movement Disorder Society. 2014;29(3):360–7. doi: 10.1002/mds.25633 . PubMed DOI PMC
Pereira JB, Ibarretxe-Bilbao N, Marti MJ, Compta Y, Junque C, Bargallo N, et al. Assessment of cortical degeneration in patients with Parkinson’s disease by voxel-based morphometry, cortical folding, and cortical thickness. Human Brain Mapping. 2012;33(11):2521–34. doi: 10.1002/hbm.21378 . PubMed DOI PMC
Mak E, Su L, Williams GB, Firbank MJ, Lawson RA, Yarnall AJ, et al. Baseline and longitudinal grey matter changes in newly diagnosed Parkinson’s disease: ICICLE-PD study. Brain: a Journal of Neurology. 2015;138(Pt 10):2974–86. doi: 10.1093/brain/awv211 . PubMed DOI PMC
Dalaker TO, Zivadinov R, Larsen JP, Beyer MK, Cox JL, Alves G, et al. Gray matter correlations of cognition in incident Parkinson’s disease. Movement Disorders: Official Journal of the Movement Disorder Society. 2010;25(5):629–33. doi: 10.1002/mds.22867 . PubMed DOI
Melzer TR, Watts R, MacAskill MR, Pitcher TL, Livingston L, Keenan RJ, et al. Grey matter atrophy in cognitively impaired Parkinson’s disease. Journal of Neurology, Neurosurgery, and Psychiatry. 2012;83(2):188–94. doi: 10.1136/jnnp-2011-300828 . PubMed DOI
Zarei M, Ibarretxe-Bilbao N, Compta Y, Hough M, Junque C, Bargallo N, et al. Cortical thinning is associated with disease stages and dementia in Parkinson’s disease. Journal of Neurology, Neurosurgery, and Psychiatry. 2013;84(8):875–81. doi: 10.1136/jnnp-2012-304126 . PubMed DOI PMC
Peran P, Cherubini A, Assogna F, Piras F, Quattrocchi C, Peppe A, et al. Magnetic resonance imaging markers of Parkinson’s disease nigrostriatal signature. Brain: a Journal of Neurology. 2010;133(11):3423–33. doi: 10.1093/brain/awq212 . PubMed DOI
Schulz JB, Skalej M, Wedekind D, Luft AR, Abele M, Voigt K, et al. Magnetic resonance imaging-based volumetry differentiates idiopathic Parkinson’s syndrome from multiple system atrophy and progressive supranuclear palsy. Annals of Neurology. 1999;45(1):65–74. . PubMed
Cordato NJ, Pantelis C, Halliday GM, Velakoulis D, Wood SJ, Stuart GW, et al. Frontal atrophy correlates with behavioural changes in progressive supranuclear palsy. Brain: a Journal of Neurology. 2002;125(Pt 4):789–800. . PubMed
Ghaemi M, Hilker R, Rudolf J, Sobesky J, Heiss WD. Differentiating multiple system atrophy from Parkinson’s disease: contribution of striatal and midbrain MRI volumetry and multi-tracer PET imaging. Journal of Neurology, Neurosurgery, and Psychiatry. 2002;73(5):517–23. doi: 10.1136/jnnp.73.5.517 . PubMed DOI PMC
Messina D, Cerasa A, Condino F, Arabia G, Novellino F, Nicoletti G, et al. Patterns of brain atrophy in Parkinson’s disease, progressive supranuclear palsy and multiple system atrophy. Parkisnonism & Related Disorders. 2011;17(3):172–6. doi: 10.1016/j.parkreldis.2010.12.010 PubMed DOI
Lee SH, Kim SS, Tae WS, Lee SY, Choi JW, Koh SB, et al. Regional volume analysis of the Parkinson disease brain in early disease stage: gray matter, white matter, striatum, and thalamus. AJNR American Journal of Neuroradiology. 2011;32(4):682–7. doi: 10.3174/ajnr.A2372 . PubMed DOI PMC
Pitcher TL, Melzer TR, Macaskill MR, Graham CF, Livingston L, Keenan RJ, et al. Reduced striatal volumes in Parkinson’s disease: a magnetic resonance imaging study. Translational Neurodegeneration. 2012;1(1):17 doi: 10.1186/2047-9158-1-17 . PubMed DOI PMC
Kosta P, Argyropoulou MI, Markoula S, Konitsiotis S. MRI evaluation of the basal ganglia size and iron content in patients with Parkinson’s disease. Journal of Neurology. 2006;253(1):26–32. doi: 10.1007/s00415-005-0914-9 . PubMed DOI
Gattellaro G, Minati L, Grisoli M, Mariani C, Carella F, Osio M, et al. White matter involvement in idiopathic Parkinson disease: a diffusion tensor imaging study. AJNR American Journal of Neuroradiology. 2009;30(6):1222–6. doi: 10.3174/ajnr.A1556 . PubMed DOI PMC
Karagulle Kendi AT, Lehericy S, Luciana M, Ugurbil K, Tuite P. Altered diffusion in the frontal lobe in Parkinson disease. AJNR American Journal of Neuroradiology. 2008;29(3):501–5. doi: 10.3174/ajnr.A0850 . PubMed DOI PMC
Rae CL, Correia MM, Altena E, Hughes LE, Barker RA, Rowe JB. White matter pathology in Parkinson’s disease: the effect of imaging protocol differences and relevance to executive function. NeuroImage. 2012;62(3):1675–84. doi: 10.1016/j.neuroimage.2012.06.012 . PubMed DOI PMC
Theilmann RJ, Reed JD, Song DD, Huang MX, Lee RR, Litvan I, et al. White-matter changes correlate with cognitive functioning in Parkinson’s disease. Frontiers in Neurology. 2013;4:37 doi: 10.3389/fneur.2013.00037 . PubMed DOI PMC
Zhan W, Kang GA, Glass GA, Zhang Y, Shirley C, Millin R, et al. Regional alterations of brain microstructure in Parkinson’s disease using diffusion tensor imaging. Movement Disorders: Official Journal of the Movement Disorder Society. 2012;27(1):90–7. doi: 10.1002/mds.23917 . PubMed DOI PMC
Duncan GW, Firbank MJ, Yarnall AJ, Khoo TK, Brooks DJ, Barker RA, et al. Gray and white matter imaging: A biomarker for cognitive impairment in early Parkinson’s disease? Movement Disorders: Official Journal of the Movement Disorder Society. 2016;31(1):103–10. doi: 10.1002/mds.26312 . PubMed DOI
Canu E, Agosta F, Sarasso E, Volonte MA, Basaia S, Stojkovic T, et al. Brain structural and functional connectivity in Parkinson’s disease with freezing of gait. Human Brain Mapping. 2015;36(12):5064–78. doi: 10.1002/hbm.22994 . PubMed DOI PMC
Bertrand JA, Bedetti C, Postuma RB, Monchi O, Genier Marchand D, Jubault T, et al. Color discrimination deficits in Parkinson’s disease are related to cognitive impairment and white-matter alterations. Movement Disorders: Official Journal of the Movement Disorder Society. 2012;27(14):1781–8. doi: 10.1002/mds.25272 . PubMed DOI
Georgiopoulos C, Warntjes M, Dizdar N, Zachrisson H, Engstrom M, Haller S, et al. Olfactory Impairment in Parkinson’s Disease Studied with Diffusion Tensor and Magnetization Transfer Imaging. Journal of Parkinson’s disease. 2017;7(2):301–11. doi: 10.3233/JPD-161060 . PubMed DOI PMC
Mishra V. S K, Zhuang X, Yang Z, Bird C, Cordes D, Walsh R. Voxelwise differences in white matter of early Parkinson’s disease (PD) subjects. OHBM; Vencouver, Canada: 2017.
Budde MD, Xie M, Cross AH, Song SK. Axial diffusivity is the primary correlate of axonal injury in the experimental autoimmune encephalomyelitis spinal cord: a quantitative pixelwise analysis. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience. 2009;29(9):2805–13. doi: 10.1523/JNEUROSCI.4605-08.2009 . PubMed DOI PMC
Teismann P, Schulz JB. Cellular pathology of Parkinson’s disease: astrocytes, microglia and inflammation. Cell and Tissue Research. 2004;318(1):149–61. doi: 10.1007/s00441-004-0944-0 . PubMed DOI
Zhang J, Aggarwal M, Mori S. Structural insights into the rodent CNS via diffusion tensor imaging. Trends in Neurosciences. 2012;35(7):412–21. doi: 10.1016/j.tins.2012.04.010 . PubMed DOI PMC
Alexander AL, Lee JE, Lazar M, Field AS. Diffusion tensor imaging of the brain. Neurotherapeutics: the journal of the American Society for Experimental NeuroTherapeutics. 2007;4(3):316–29. doi: 10.1016/j.nurt.2007.05.011 . PubMed DOI PMC
Picconi B, Piccoli G, Calabresi P. Synaptic dysfunction in Parkinson’s disease. Advances in Experimental Medicine and Biology. 2012;970:553–72. doi: 10.1007/978-3-7091-0932-8_24 . PubMed DOI
Tessitore A, Giordano A, Russo A, Tedeschi G. Structural connectivity in Parkinson’s disease. Parkinsonism & Related Disorders. 2016;22 Suppl 1:S56–9. doi: 10.1016/j.parkreldis.2015.09.018 . PubMed DOI
Braak H, Sandmann-Keil D, Gai W, Braak E. Extensive axonal Lewy neurites in Parkinson’s disease: a novel pathological feature revealed by alpha-synuclein immunocytochemistry. Neuroscience Letters. 1999;265(1):67–9. . PubMed
Tessitore A, Esposito F, Vitale C, Santangelo G, Amboni M, Russo A, et al. Default-mode network connectivity in cognitively unimpaired patients with Parkinson disease. Neurology. 2012;79(23):2226–32. doi: 10.1212/WNL.0b013e31827689d6 . PubMed DOI
Rektor I, Goldemund D, Bednarik P, Sheardova K, Michalkova Z, Telecka S, et al. Impairment of brain vessels may contribute to mortality in patients with Parkinson’s disease. Movement Disorders: Official Journal of the Movement Disorder Society. 2012;27(9):1169–72. doi: 10.1002/mds.25066 . PubMed DOI
Vesely B, Antonini A, Rektor I. The contribution of white matter lesions to Parkinson’s disease motor and gait symptoms: a critical review of the literature. Journal of Neural Transmission. 2016;123(3):241–50. doi: 10.1007/s00702-015-1470-9 . PubMed DOI
Ham JH, Yun HJ, Sunwoo MK, Hong JY, Lee JM, Sohn YH, et al. Topography of cortical thinning associated with white matter hyperintensities in Parkinson’s disease. Parkinsonism & Related Disorders. 2015;21(4):372–7. doi: 10.1016/j.parkreldis.2015.01.015 . PubMed DOI
Sunwoo MK, Jeon S, Ham JH, Hong JY, Lee JE, Lee JM, et al. The burden of white matter hyperintensities is a predictor of progressive mild cognitive impairment in patients with Parkinson’s disease. European Journal of Neurology. 2014;21(6):922–e50. doi: 10.1111/ene.12412 . PubMed DOI
Zhang Y, Wu IW, Tosun D, Foster E, Schuff N, Parkinson’s Progression Markers I. Progression of Regional Microstructural Degeneration in Parkinson’s Disease: A Multicenter DiffusionTensorImagingStudy. PloSOne.2016;11(10):e0165540 doi: 10.1371/journal.pone.0165540 . PubMed DOI PMC
Agosta F, Canu E, Stefanova E, Sarro L, Tomic A, Spica V, et al. Mild cognitive impairment in Parkinson’s disease is associated with a distributed pattern of brain white matter damage. Human Brain Mapping. 2014;35(5):1921–9. doi: 10.1002/hbm.22302 . PubMed DOI PMC
Alves GS, Oertel Knochel V, Knochel C, Carvalho AF, Pantel J, Engelhardt E, et al. Integrating retrogenesis theory to Alzheimer’s disease pathology: insight from DTI-TBSS investigation of the white matter microstructural integrity. BioMed Research International. 2015;2015:291658 doi: 10.1155/2015/291658 . PubMed DOI PMC
Dyrby TB, Lundell H, Burke MW, Reislev NL, Paulson OB, Ptito M, et al. Interpolation of diffusion weighted imaging datasets. NeuroImage. 2014;103:202–13. doi: 10.1016/j.neuroimage.2014.09.005 . PubMed DOI
Smith SM, Johansen-Berg H, Jenkinson M, Rueckert D, Nichols TE, Miller KL, et al. Acquisition and voxelwise analysis of multi-subject diffusion data with tract-based spatial statistics. Nature Protocols. 2007;2(3):499–503. doi: 10.1038/nprot.2007.45 . PubMed DOI
Jones DK, Cercignani M. Twenty-five pitfalls in the analysis of diffusion MRI data. NMR in Biomedicine. 2010;23(7):803–20. doi: 10.1002/nbm.1543 . PubMed DOI