Diffusion tensor imaging in Alzheimer's disease: Insights into the limbic-diencephalic network and methodological considerations

Frontiers in Aging Neuroscience

Volumn 6, Issue SEP, 2014, Pages

  Acosta Cabronero, Julio ^a   Nestor, Peter J ^a  

^a GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

ADNI; Alzheimer's disease biomarkers; Alzheimer's disease neurobiology; Alzheimer's disease pathomechanisms; Autosomal dominant Alzheimer's disease mutation; Axial diffusivity; Axonal loss; B value; Cingulum; Circuit of Papez; Commissural tracts; Corona radiata; Corpus callosum; Demyelination; Diffusion directions; Diffusion path; Diffusion regimes; Diffusion tensor dynamics; Diffusion time; DTI criteria; Forceps major; Genu; Glial pathology; Hippocampus; Inter hemispheric tracts; Limbic tracts; Long association tracts; Mean diffusivity; Mild cognitive impairment; Neurodegenerative diseases; Neuronal damage; Non parametric statistics; Parahippocampal white matter; Permutation statistics; Posterior cingulate; Preclinical AD; PSEN1; Sagittal stratum; Single shot echo planar imaging; Splenium; Subjective cognitive impairment

Indexed keywords

ALZHEIMER DISEASE; ARTICLE; BEHAVIOR; BRAIN FORNIX; BRAIN REGION; CLINICAL FEATURE; DEGENERATIVE DISEASE; DIENCEPHALON; DIFFUSION TENSOR IMAGING; DISEASE SEVERITY; FRACTIONAL ANISOTROPY; HUMAN; IMAGE ANALYSIS; IMAGE PROCESSING; IMAGE QUALITY; LIMBIC CORTEX; LIMBIC DIENCEPHALIC NETWORK; MATHEMATICAL PARAMETERS; MULTICENTER STUDY (TOPIC); NERVE CELL NETWORK; NEUROPATHOLOGY; PHYSICAL PHENOMENA; PRACTICE GUIDELINE; RADIOLOGICAL PARAMETERS; SENSITIVITY ANALYSIS; TEMPORAL LOBE;

EID: 84907181861     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2014.00266     Document Type: Article

References (99)

1. Aboitiz, F., Scheibel, A.B., Fisher, R.S., and Zaidel, E. (1992). Fiber composition of the human corpus callosum. Brain Res 598, 143-153
2. Acosta-Cabronero, J., Alley, S., Williams, G.B., Pengas, G., and Nestor, P.J. (2012). Diffusion tensor metrics as biomarkers in Alzheimer's disease. PLoS One 7, e49072. doi: 10.1371/journal.pone.0049072
3. Acosta-Cabronero, J., Williams, G.B., Pengas, G., and Nestor, P.J. (2010). Absolute diffusivities define the landscape of white matter degeneration in Alzheimer's disease. Brain 133, 529-539
4. Alexander, D.C., and Barker, G.J. (2005). Optimal imaging parameters for fiber-orientation estimation in diffusion MRI. Neuroimage 27, 357-367. doi: 10.1016/j.neuroimage.2005.04.008
5. Alger, J.R. (2012). The diffusion tensor imaging toolbox. J Neurosci 32, 7418-7428. doi: 10.1523/JNEUROSCI.4687-11.2012
6. Ashburner, J., and Friston, K.J. (2000). Voxel-based morphometry--the methods. Neuroimage 11, 805-821
7. Assaf, Y., and Basser, P.J. (2005). Composite hindered and restricted model of diffusion (CHARMED) MR imaging of the human brain. Neuroimage 27, 48-58. doi: 10.1016/j.neuroimage.2005.03.042
8. Avants, B.B., Epstein, C.L., Grossman, M., and Gee, J.C. (2008). Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal 12, 26-41. doi: 10.1016/j.media.2007.06.004
9. Balachandar, R., John, J.P., Saini, J., Kumar, K.J., Joshi, H., Sadanand, S., Aiyappan, S., Sivakumar, P.T., Loganathan, S., Varghese, M., and Bharath, S. (in press). A study of structural and functional connectivity in early Alzheimer's disease using rest fMRI and diffusion tensor imaging. Int J Geriatr Psychiatry. doi: 10.1002/gps.4168
10. Baron, C.A., and Beaulieu, C. (2013). Oscillating Gradient Spin-Echo (OGSE) diffusion tensor imaging of the human brain. Magn Reson Med. doi: 10.1002/mrm.24987
11. Basser, P.J., Mattiello, J., and Lebihan, D. (1994a). Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 103, 247-254
12. Basser, P.J., Mattiello, J., and Lebihan, D. (1994b). MR diffusion tensor spectroscopy and imaging. Biophys J 66, 259-267
13. Basser, P.J., and Pierpaoli, C. (1996). Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 111, 209-219
14. Batchelor, P.G., Atkinson, D., Hill, D.L., Calamante, F., and Connelly, A. (2003). Anisotropic noise propagation in diffusion tensor MRI sampling schemes. Magn Reson Med 49, 1143-1151. doi: 10.1002/mrm.10491
15. Beaulieu, C. (2002). The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed 15, 435-455
16. Beaulieu, C., and Allen, P.S. (1994). Water diffusion in the giant axon of the squid: implications for diffusion-weighted MRI of the nervous system. Magn Reson Med 32, 579-583
17. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57, 289-300. doi: doi: 10.2307/2346101
18. Besseling, R.M., Jansen, J.F., Overvliet, G.M., Vaessen, M.J., Braakman, H.M., Hofman, P.A., Aldenkamp, A.P., and Backes, W.H. (2012). Tract specific reproducibility of tractography based morphology and diffusion metrics. PLoS One 7, e34125. doi: 10.1371/journal.pone.0034125
19. Bosch, B., Arenaza-Urquijo, E.M., Rami, L., Sala-Llonch, R., Junque, C., Sole-Padulles, C., Pena-Gomez, C., Bargallo, N., Molinuevo, J.L., and Bartres-Faz, D. (2012). Multiple DTI index analysis in normal aging, amnestic MCI and AD. Relationship with neuropsychological performance. Neurobiol Aging 33, 61-74
20. Brown, R. (1828). Microscopical observations of active molecules. Edinburgh New Philosophical Journal July-September, 358-371. doi: citeulike-article-id:1007061
21. Canu, E., Agosta, F., Spinelli, E.G., Magnani, G., Marcone, A., Scola, E., Falautano, M., Comi, G., Falini, A., and Filippi, M. (2013). White matter microstructural damage in Alzheimer's disease at different ages of onset. Neurobiol Aging 34, 2331-2340. doi: 10.1016/j.neurobiolaging.2013.03.026
22. Carr, H.Y., and Purcell, E.M. (1954). Effects of diffusion on free precession in nuclear magnetic resonance experiments. Phys Rev 94, 630-638
23. Choo, 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., and Woo, J.I. (2010). Posterior cingulate cortex atrophy and regional cingulum disruption in mild cognitive impairment and Alzheimer's disease. Neurobiol Aging 31, 772-779
24. Clark, C.M., Pontecorvo, M.J., Beach, T.G., Bedell, B.J., Coleman, R.E., Doraiswamy, P.M., Fleisher, A.S., Reiman, E.M., Sabbagh, M.N., Sadowsky, C.H., Schneider, J.A., Arora, A., Carpenter, A.P., Flitter, M.L., Joshi, A.D., Krautkramer, M.J., Lu, M., Mintun, M.A., Skovronsky, D.M., and Group, A.-a.S. (2012). Cerebral PET with florbetapir compared with neuropathology at autopsy for detection of neuritic amyloid-beta plaques: a prospective cohort study. Lancet Neurol 11, 669-678. doi: 10.1016/S1474-4422(12)70142-4
25. Coleman, M.P., and Freeman, M.R. (2010). Wallerian degeneration, wld(s), and nmnat. Annu Rev Neurosci 33, 245-267. doi: 10.1146/annurev-neuro-060909-153248
26. Correia, M.M., Carpenter, T.A., and Williams, G.B. (2009). Looking for the optimal DTI acquisition scheme given a maximum scan time: are more b-values a waste of time? Magn Reson Imaging 27, 163-175. doi: 10.1016/j.mri.2008.06.011
27. Dale, A.M., Fischl, B., and Sereno, M.I. (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9, 179-194. doi: 10.1006/nimg.1998.0395
28. Damoiseaux, J.S., Smith, S.M., Witter, M.P., Sanz-Arigita, E.J., Barkhof, F., Scheltens, P., Stam, C.J., Zarei, M., and Rombouts, S.A. (2009). White matter tract integrity in aging and Alzheimer's disease. Hum Brain Mapp 30, 1051-1059. doi: 10.1002/hbm.20563
29. Diaz-De-Grenu, L.Z., Acosta-Cabronero, J., Chong, Y.F., Pereira, J.M., Sajjadi, S.A., Williams, G.B., and Nestor, P.J. (2014). A brief history of voxel-based grey matter analysis in Alzheimer's disease. J Alzheimers Dis 38, 647-659. doi: 10.3233/JAD-130362
30. Douaud, G., Jbabdi, S., Behrens, T.E., Menke, R.A., Gass, A., Monsch, A.U., Rao, A., Whitcher, B., Kindlmann, G., Matthews, P.M., and Smith, S. (2011). DTI measures in crossing-fibre areas: increased diffusion anisotropy reveals early white matter alteration in MCI and mild Alzheimer's disease. Neuroimage 55, 880-890. doi: 10.1016/j.neuroimage.2010.12.008
31. Du, A.T., Schuff, N., Amend, D., Laakso, M.P., Hsu, Y.Y., Jagust, W.J., Yaffe, K., Kramer, J.H., Reed, B., Norman, D., Chui, H.C., and Weiner, M.W. (2001). Magnetic resonance imaging of the entorhinal cortex and hippocampus in mild cognitive impairment and Alzheimer's disease. J Neurol Neurosurg Psychiatry 71, 441-447
32. Edden, R.A., and Jones, D.K. (2011). Spatial and orientational heterogeneity in the statistical sensitivity of skeleton-based analyses of diffusion tensor MR imaging data. J Neurosci Methods 201, 213-219. doi: 10.1016/j.jneumeth.2011.07.025
33. Einstein, A. (1905). U¨ber die von der molekularkinetischen Theorie der Wa¨rme geforderte Bewegung von in ruhenden Flu¨ssigkeiten suspendierten Teilchen. Ann Phys 322, 549-560. doi: 10.1002/andp.19053220806
34. Fazekas, F., Chawluk, J.B., Alavi, A., Hurtig, H.I., and Zimmerman, R.A. (1987). MR signal abnormalities at 1.5 T in Alzheimer's dementia and normal aging. AJR Am J Roentgenol 149, 351-356
35. Fick, A. (1855). Ueber Diffusion. Ann Phys 170, 59-86. doi: 10.1002/andp.18551700105
36. Fieremans, E., Benitez, A., Jensen, J.H., Falangola, M.F., Tabesh, A., Deardorff, R.L., Spampinato, M.V., Babb, J.S., Novikov, D.S., Ferris, S.H., and Helpern, J.A. (2013). Novel white matter tract integrity metrics sensitive to Alzheimer disease progression. AJNR Am J Neuroradiol 34, 2105-2112. doi: 10.3174/ajnr.A3553
37. Fischl, B., Sereno, M.I., and Dale, A.M. (1999). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage 9, 195-207. doi: 10.1006/nimg.1998.0396
38. Folstein, M.F., Folstein, S.E., and Mchugh, P.R. (1975). Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12, 189-198
39. Frost, R., Jezzard, P., Douaud, G., Clare, S., Porter, D.A., and Miller, K.L. (in press). Scan time reduction for readout-segmented EPI using simultaneous multislice acceleration: Diffusionweighted imaging at 3 and 7 Tesla. Magn Reson Med. doi: 10.1002/mrm.25391
40. Griswold, M.A., Jakob, P.M., Heidemann, R.M., Nittka, M., Jellus, V., Wang, J., Kiefer, B., and Haase, A. (2002). Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med 47, 1202-1210
41. Hahn, E.L. (1950). Spin echoes. Physical Review 80, 580-594
42. Huang, H., Fan, X., Weiner, M., Martin-Cook, K., Xiao, G., Davis, J., Devous, M., Rosenberg, R., and Diaz-Arrastia, R. (2012). Distinctive disruption patterns of white matter tracts in Alzheimer's disease with full diffusion tensor characterization. Neurobiol Aging 33, 2029-2045. doi: 10.1016/j.neurobiolaging.2011.06.027
43. Ishii, K., Sasaki, H., Kono, A.K., Miyamoto, N., Fukuda, T., and Mori, E. (2005). Comparison of gray matter and metabolic reduction in mild Alzheimer's disease using FDG-PET and voxelbased morphometric MR studies. Eur J Nucl Med Mol Imaging 32, 959-963. doi: 10.1007/s00259-004-1740-5
44. Jack, C.R., Jr., Bernstein, M.A., Borowski, B.J., Gunter, J.L., Fox, N.C., Thompson, P.M., Schuff, N., Krueger, G., Killiany, R.J., Decarli, C.S., Dale, A.M., Carmichael, O.W., Tosun, D., Weiner, M.W., and Alzheimer's Disease Neuroimaging, I. (2010). Update on the magnetic resonance imaging core of the Alzheimer's disease neuroimaging initiative. Alzheimers Dement 6, 212-220. doi: 10.1016/j.jalz.2010.03.004
45. Jack, C.R., Jr., Dickson, D.W., Parisi, J.E., Xu, Y.C., Cha, R.H., O'brien, P.C., Edland, S.D., Smith, G.E., Boeve, B.F., Tangalos, E.G., Kokmen, E., and Petersen, R.C. (2002). Antemortem MRI findings correlate with hippocampal neuropathology in typical aging and dementia. Neurology 58, 750-757
46. Jack, C.R., Jr., Shiung, M.M., Gunter, J.L., O'brien, P.C., Weigand, S.D., Knopman, D.S., Boeve, B.F., Ivnik, R.J., Smith, G.E., Cha, R.H., Tangalos, E.G., and Petersen, R.C. (2004). Comparison of different MRI brain atrophy rate measures with clinical disease progression in AD. Neurology 62, 591-600
47. Jbabdi, S., Behrens, T.E., and Smith, S.M. (2010). Crossing fibres in tract-based spatial statistics. Neuroimage 49, 249-256. doi: 10.1016/j.neuroimage.2009.08.039
48. Jensen, J.H., Helpern, J.A., Ramani, A., Lu, H., and Kaczynski, K. (2005). Diffusional kurtosis imaging: the quantification of non-gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med 53, 1432-1440. doi: 10.1002/mrm.20508
49. Jicha, G.A., Parisi, J.E., Dickson, D.W., Johnson, K., Cha, R., Ivnik, R.J., Tangalos, E.G., Boeve, B.F., Knopman, D.S., Braak, H., and Petersen, R.C. (2006). Neuropathologic outcome of mild cognitive impairment following progression to clinical dementia. Arch Neurol 63, 674-681. doi: 10.1001/archneur.63.5.674
50. Jones, D.K. (2004). The effect of gradient sampling schemes on measures derived from diffusion tensor MRI: a Monte Carlo study. Magn Reson Med 51, 807-815. doi: 10.1002/mrm.20033
51. Jones, D.K., and Cercignani, M. (2010). Twenty-five pitfalls in the analysis of diffusion MRI data. NMR Biomed 23, 803-820. doi: 10.1002/nbm.1543
52. Jones, D.K., Christiansen, K.F., Chapman, R.J., and Aggleton, J.P. (2013a). Distinct subdivisions of the cingulum bundle revealed by diffusion MRI fibre tracking: implications for neuropsychological investigations. Neuropsychologia 51, 67-78. doi: 10.1016/j.neuropsychologia.2012.11.018
53. Jones, D.K., Knosche, T.R., and Turner, R. (2013b). White matter integrity, fiber count, and other fallacies: the do's and don'ts of diffusion MRI. Neuroimage 73, 239-254. doi: 10.1016/j.neuroimage.2012.06.081
54. Keihaninejad, S., Ryan, N.S., Malone, I.B., Modat, M., Cash, D., Ridgway, G.R., Zhang, H., Fox, N.C., and Ourselin, S. (2012). The importance of group-wise registration in tract based spatial statistics study of neurodegeneration: a simulation study in Alzheimer's disease. PLoS One 7, e45996. doi: 10.1371/journal.pone.0045996
55. Keihaninejad, S., Zhang, H., Ryan, N.S., Malone, I.B., Modat, M., Cardoso, M.J., Cash, D.M., Fox, N.C., and Ourselin, S. (2013). An unbiased longitudinal analysis framework for tracking white matter changes using diffusion tensor imaging with application to Alzheimer's disease. NeuroImage 72, 153-163. doi: http://dx.doi.org/10.1016/j.neuroimage.2013.01.044
56. Kingsley, P.B. (2006a). Introduction to diffusion tensor imaging mathematics: Part I. Tensors, rotations, and eigenvectors. Concept Magn Reson A 28A, 101-122. doi: 10.1002/cmr.a.20048
57. Kingsley, P.B. (2006b). Introduction to diffusion tensor imaging mathematics: Part II. Anisotropy, diffusion-weighting factors, and gradient encoding schemes. Concept Magn Reson A 28A, 123-154. doi: 10.1002/cmr.a.20049
58. Kingsley, P.B. (2006c). Introduction to diffusion tensor imaging mathematics: Part III. Tensor calculation, noise, simulations, and optimization. Concept Magn Reson A 28A, 155-179. doi: 10.1002/cmr.a.20050
59. Klein, A., Andersson, J., Ardekani, B.A., Ashburner, J., Avants, B., Chiang, M.C., Christensen, G.E., Collins, D.L., Gee, J., Hellier, P., Song, J.H., Jenkinson, M., Lepage, C., Rueckert, D., Thompson, P., Vercauteren, T., Woods, R.P., Mann, J.J., and Parsey, R.V. (2009). Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration. Neuroimage 46, 786-802. doi: 10.1016/j.neuroimage.2008.12.037
60. Leemans, A., and Jones, D.K. (2009). The B-matrix must be rotated when correcting for subject motion in DTI data. Magn Reson Med 61, 1336-1349. doi: 10.1002/mrm.21890
61. Lim, J.S., Park, Y.H., Jang, J.W., Park, S.Y., Kim, S., and Alzheimer's Disease Neuroimaging, I. (2014). Differential white matter connectivity in early mild cognitive impairment according to CSF biomarkers. PLoS One 9, e91400. doi: 10.1371/journal.pone.0091400
62. Mahoney, C.J., Malone, I.B., Ridgway, G.R., Buckley, A.H., Downey, L.E., Golden, H.L., Ryan, N.S., Ourselin, S., Schott, J.M., Rossor, M.N., Fox, N.C., and Warren, J.D. (2013). White matter tract signatures of the progressive aphasias. Neurobiol Aging 34, 1687-1699. doi: 10.1016/j.neurobiolaging.2012.12.002
63. McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., and Stadlan, E.M. (1984). Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 34, 939-944
64. Minoshima, S., Frey, K.A., Koeppe, R.A., Foster, N.L., and Kuhl, D.E. (1995). A diagnostic approach in Alzheimer's disease using three-dimensional stereotactic surface projections of fluorine-18-FDG PET. J Nucl Med 36, 1238-1248
65. Minoshima, S., Giordani, B., Berent, S., Frey, K.A., Foster, N.L., and Kuhl, D.E. (1997). Metabolic reduction in the posterior cingulate cortex in very early Alzheimer's disease. Ann Neurol 42, 85-94
66. Mitchell, J., Arnold, R., Dawson, K., Nestor, P.J., and Hodges, J.R. (2009). Outcome in subgroups of mild cognitive impairment (MCI) is highly predictable using a simple algorithm. J Neurol 256, 1500-1509. doi: http://dx.doi.org/10.1007/s00415-009-5152-0
67. Molinuevo, J.L., Ripolles, P., Simo, M., Llado, A., Olives, J., Balasa, M., Antonell, A., Rodriguez-Fornells, A., and Rami, L. (in press). White matter changes in preclinical Alzheimer's disease: a magnetic resonance imaging-diffusion tensor imaging study on cognitively normal older people with positive amyloid beta protein 42 levels. Neurobiol Aging. doi: 10.1016/j.neurobiolaging.2014.05.027
68. Nestor, P.J., Fryer, T.D., and Hodges, J.R. (2006). Declarative memory impairments in Alzheimer's disease and semantic dementia. Neuroimage 30, 1010-1020
69. Nestor, P.J., Fryer, T.D., Ikeda, M., and Hodges, J.R. (2003a). Retrosplenial cortex (BA 29/30) hypometabolism in mild cognitive impairment (prodromal Alzheimer's disease). Eur J Neurosci 18, 2663-2667
70. Nestor, P.J., Fryer, T.D., Smielewski, P., and Hodges, J.R. (2003b). Limbic hypometabolism in Alzheimer's disease and mild cognitive impairment. Ann Neurol 54, 343-351. doi: 10.1002/ana.10669
71. Nir, T.M., Jahanshad, N., Villalon-Reina, J.E., Toga, A.W., Jack, C.R., Weiner, M.W., Thompson, P.M., and Alzheimer's Disease Neuroimaging, I. (2013). Effectiveness of regional DTI measures in distinguishing Alzheimer's disease, MCI, and normal aging. Neuroimage Clin 3, 180-195. doi: 10.1016/j.nicl.2013.07.006
72. Oishi K and Lyketsos C (2014). Alzheimer's disease and the fornix. Front Aging Neurosci 6, 241. doi: 10.3389/fnagi.2014.00241
73. Oouchi, H., Yamada, K., Sakai, K., Kizu, O., Kubota, T., Ito, H., and Nishimura, T. (2007). Diffusion anisotropy measurement of brain white matter is affected by voxel size: underestimation occurs in areas with crossing fibers. AJNR Am J Neuroradiol 28, 1102-1106. doi: 10.3174/ajnr.A0488
74. Papadakis, N.G., Murrills, C.D., Hall, L.D., Huang, C.L., and Carpenter, A.T. (2000). Minimal gradient encoding for robust estimation of diffusion anisotropy. Magn Reson Imaging 18, 671-679
75. Papez, J.W. (1937). A proposed mechanism of emotion. Arch Neurol Psychiatry 38, 725-743. doi: 10.1001/archneurpsyc.1937.02260220069003
76. Pasternak, O., Sochen, N., Gur, Y., Intrator, N., and Assaf, Y. (2009). Free water elimination and mapping from diffusion MRI. Magn Reson Med 62, 717-730. doi: 10.1002/mrm.22055
77. Pengas, G., Hodges, J.R., Watson, P., and Nestor, P.J. (2010). Focal posterior cingulate atrophy in incipient Alzheimer's disease. Neurobiol Aging 31, 25-33
78. Pengas, G., Williams, G.B., Acosta-Cabronero, J., Ash, T.W., Hong, Y.T., Izquierdo-Garcia, D., Fryer, T.D., Hodges, J.R., and Nestor, P.J. (2012). The relationship of topographical memory performance to regional neurodegeneration in Alzheimer's disease. Front Aging Neurosci 4, 17. doi: 10.3389/fnagi.2012.00017
79. Pruessmann, K.P., Weiger, M., Scheidegger, M.B., and Boesiger, P. (1999). SENSE: sensitivity encoding for fast MRI. Magn Reson Med 42, 952-962
80. Racine, A.M., Adluru, N., Alexander, A.L., Christian, B.T., Okonkwo, O.C., Oh, J., Cleary, C.A., Birdsill, A., Hillmer, A.T., Murali, D., Barnhart, T.E., Gallagher, C.L., Carlsson, C.M., Rowley, H.A., Dowling, N.M., Asthana, S., Sager, M.A., Bendlin, B.B., and Johnson, S.C. (2014). Associations between white matter microstructure and amyloid burden in preclinical Alzheimer's disease: A multimodal imaging investigation. NeuroImage: Clinical 4, 604-614. doi: http://dx.doi.org/10.1016/j.nicl.2014.02.001
81. Rowley, J., Fonov, V., Wu, O., Eskildsen, S.F., Schoemaker, D., Wu, L., Mohades, S., Shin, M., Sziklas, V., Cheewakriengkrai, L., Shmuel, A., Dagher, A., Gauthier, S., Rosa-Neto, P., and Alzheimer's Disease Neuroimaging, I. (2013). White matter abnormalities and structural hippocampal disconnections in amnestic mild cognitive impairment and Alzheimer's disease. PLoS One 8, e74776. doi: 10.1371/journal.pone.0074776
82. Ryan, N.S., Keihaninejad, S., Shakespeare, T.J., Lehmann, M., Crutch, S.J., Malone, I.B., Thornton, J.S., Mancini, L., Hyare, H., Yousry, T., Ridgway, G.R., Zhang, H., Modat, M., Alexander, D.C., Rossor, M.N., Ourselin, S., and Fox, N.C. (2013). Magnetic resonance imaging evidence for presymptomatic change in thalamus and caudate in familial Alzheimer's disease. Brain 136, 1399-1414. doi: 10.1093/brain/awt065
83. Schwarz, C.G., Reid, R.I., Gunter, J.L., Senjem, M.L., Przybelski, S.A., Zuk, S.M., Whitwell, J.L., Vemuri, P., Josephs, K.A., Kantarci, K., Thompson, P.M., Petersen, R.C., Jack, C.R., Jr., and Alzheimer's Disease Neuroimaging, I. (2014). Improved DTI registration allows voxel-based analysis that outperforms tract-based spatial statistics. Neuroimage 94, 65-78. doi: 10.1016/j.neuroimage.2014.03.026
84. Smith, S.M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T.E., Mackay, C.E., Watkins, K.E., Ciccarelli, O., Cader, M.Z., Matthews, P.M., and Behrens, T.E. (2006). Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31, 1487-1505. doi: 10.1016/j.neuroimage.2006.02.024
85. Smith, S.M., Jenkinson, M., Woolrich, M.W., Beckmann, C.F., Behrens, T.E., Johansen-Berg, H., Bannister, P.R., De Luca, M., Drobnjak, I., Flitney, D.E., Niazy, R.K., Saunders, J., Vickers, J., Zhang, Y., De Stefano, N., Brady, J.M., and Matthews, P.M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23 Suppl 1, S208-219
86. Smith, S.M., and Nichols, T.E. (2009). Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44, 83-98. doi: 10.1016/j.neuroimage.2008.03.061
87. Stejskal, E.O., and Tanner, J.E. (1965). Spin diffusion measurements: spin echoes in the presence of a time-dependent field gradient. J Chem Phys 42, 288-292. doi: http://dx.doi.org/10.1063/1.1695690
88. Teipel, S.J., Reuter, S., Stieltjes, B., Acosta-Cabronero, J., Ernemann, U., Fellgiebel, A., Filippi, M., Frisoni, G., Hentschel, F., Jessen, F., Kloppel, S., Meindl, T., Pouwels, P.J., Hauenstein, K.H., and Hampel, H. (2011). Multicenter stability of diffusion tensor imaging measures: a European clinical and physical phantom study. Psychiatry Res 194, 363-371. doi: 10.1016/j.pscychresns.2011.05.012
89. Torrey, H.C. (1956). Bloch equations with diffusion terms. Phys Rev 104, 563-565
90. Tuch, D.S. (2004). Q-ball imaging. Magn Reson Med 52, 1358-1372. doi: 10.1002/mrm.20279
91. Verwey, N.A., Van Der Flier, W.M., Blennow, K., Clark, C., Sokolow, S., De Deyn, P.P., Galasko, D., Hampel, H., Hartmann, T., Kapaki, E., Lannfelt, L., Mehta, P.D., Parnetti, L., Petzold, A., Pirttila, T., Saleh, L., Skinningsrud, A., Swieten, J.C., Verbeek, M.M., Wiltfang, J., Younkin, S., Scheltens, P., and Blankenstein, M.A. (2009). A worldwide multicentre comparison of assays for cerebrospinal fluid biomarkers in Alzheimer's disease. Ann Clin Biochem 46, 235-240. doi: 10.1258/acb.2009.008232
92. Villemagne, V.L., Pike, K.E., Che´telat, G., Ellis, K.A., Mulligan, R.S., Bourgeat, P., Ackermann, U., Jones, G., Szoeke, C., Salvado, O., Martins, R., O'keefe, G., Mathis, C.A., Klunk, W.E., Ames, D., Masters, C.L., and Rowe, C.C. (2011). Longitudinal assessment of Aβ and cognition in aging and Alzheimer disease. Ann Neurol 69, 181-192. doi: 10.1002/ana.22248
93. Wedeen, V.J., Hagmann, P., Tseng, W.Y., Reese, T.G., and Weisskoff, R.M. (2005). Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn Reson Med 54, 1377-1386. doi: 10.1002/mrm.20642
94. Winkler, A.M., Ridgway, G.R., Webster, M.A., Smith, S.M., and Nichols, T.E. (2014). Permutation inference for the general linear model. Neuroimage 92, 381-397. doi: 10.1016/j.neuroimage.2014.01.060
95. Winston, G.P. (2012). The physical and biological basis of quantitative parameters derived from diffusion MRI. Quant Imaging Med Surg 2, 254-265. doi: 10.3978/j.issn.2223-4292.2012.12.05
96. Xing, D., Papadakis, N.G., Huang, C.L., Lee, V.M., Carpenter, T.A., and Hall, L.D. (1997). Optimised diffusion-weighting for measurement of apparent diffusion coefficient (ADC) in human brain. Magn Reson Imaging 15, 771-784
97. Zarei, M., Damoiseaux, J.S., Morgese, C., Beckmann, C.F., Smith, S.M., Matthews, P.M., Scheltens, P., Rombouts, S.A., and Barkhof, F. (2009). Regional white matter integrity differentiates between vascular dementia and Alzheimer disease. Stroke 40, 773-779. doi: 10.1161/STROKEAHA.108.530832
98. Zhang, H., Schneider, T., Wheeler-Kingshott, C.A., and Alexander, D.C. (2012). NODDI: practical in vivo neurite orientation dispersion and density imaging of the human brain. Neuroimage 61, 1000-1016. doi: 10.1016/j.neuroimage.2012.03.072
99. Zhang, H., Yushkevich, P.A., Alexander, D.C., and Gee, J.C. (2006). Deformable registration of diffusion tensor MR images with explicit orientation optimization. Med Image Anal 10, 764-785. doi: 10.1016/j.media.2006.06.004.