The role of tissue microstructure and water exchange in biophysical modelling of diffusion in white matter

Magnetic Resonance Materials in Physics, Biology and Medicine

Volumn 26, Issue 4, 2013, Pages 345-370

  Nilsson, Markus ^a   Van Westen, Danielle ^a   Ståhlberg, Freddy ^a   Sundgren, Pia C ^a   Lätt, Jimmy ^b  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Diffusion weighted imaging; Exchange; Microstructure; Permeability; White matter

Indexed keywords

ANIMALIA;

EID: 84881318622     PISSN: 09685243     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10334-013-0371-x     Document Type: Review

References (189)

1. Minati L, Weglarz W (2007) Physical foundations, models, and methods of diffusion magnetic resonance imaging of the brain: a review. Concepts Magn Reson Part A Bridge Educt Res 30(5):278-307
2. Price W (1997) Pulsed-field gradient nuclear magnetic resonance as a tool for studying translational diffusion: part 1. Basic theory. Concepts Magn Reson Part A Bridge Educt Res 9:299-336 (Pubitemid 127116750)
3. Stejskal EO, Tanner JE (1965) Spin diffusion measurements: spin echoes in the presence of a time-dependent field gradient. J Chem Phys 42(1):288-292
4. Stejskal EO (1965) Use of spin echoes in a pulsed magnetic-field gradient to study anisotropic, restricted diffusion and flow. J Chem Phys 43:3597
5. Cory DG, Garroway AN, Miller JB (1990) Applications of spin transport as a probe of local geometry. Polym Prepr 31:149
6. Mitra P (1995) Multiple wave-vector extensions of the NMR pulsed-field-gradient spin-echo diffusion measurement. Phys Rev B 51(21):15074-15078
7. Callaghan P, Komlosh M (2002) Locally anisotropic motion in a macroscopically isotropic system: displacement correlations measured using double pulsed gradient spin-echo NMR. Magn Reson Chem 40(13):S15-S19 (Pubitemid 37296910)
8. Komlosh ME, Horkay F, Freidlin RZ, Nevo U, Assaf Y, Basser PJ (2007) Detection of microscopic anisotropy in gray matter and in a novel tissue phantom using double pulsed gradient spin echo MR. J Magn Reson 189(1):38-45 (Pubitemid 350026791)
9. Özarslan E, Basser PJ (2008) Microscopic anisotropy revealed by NMR double pulsed field gradient experiments with arbitrary timing parameters. J Chem Phys 128(15):154511 (Pubitemid 351574657)
10. Shemesh N, Ozarslan E, Komlosh ME, Basser PJ, Cohen Y (2010) From single-pulsed field gradient to double-pulsed field gradient MR: gleaning new microstructural information and developing new forms of contrast in MRI. NMR Biomed 23(7):757-780
11. Koch MA, Finsterbusch J (2008) Compartment size estimation with double wave vector diffusion-weighted imaging. Magn Reson Med 60(1):90-101 (Pubitemid 351956613)
12. Callaghan PT, Furó I (2004) Diffusion-diffusion correlation and exchange as a signature for local order and dynamics. J Chem Phys 120(8):4032-4038
13. Åslund I, Nowacka A, Nilsson M, Topgaard D (2009) Filter-exchange PGSE NMR determination of cell membrane permeability. J Magn Reson 200(2):291-295
14. Callaghan PT, Stepisnik J (1995) Frequency-domain analysis of spin motion using modulated-gradient NMR. J Magn Reson A 117(1):118-122
15. Gross B, Kosfeld R (1969) Anwendung der spin-echo-methode der messung der selbstdiffusion. Messtechnik 77:171-177
16. Stepisnik J (1981) Analysis of NMR self-diffusion measurements by a density matrix calculation. Phys B 104(3):350-364 (Pubitemid 12462259)
17. Schachter M, Does MD, Anderson AW, Gore JC (2000) Measurements of restricted diffusion using an oscillating gradient spin-echo sequence. J Magn Reson 147(2):232-237
18. Drobnjak I, Siow B, Alexander DC (2010) Optimizing gradient waveforms for microstructure sensitivity in diffusion-weighted MR. J Magn Reson 206(1):41-51
19. Alexander DC (2008) A general framework for experiment design in diffusion MRI and its application in measuring direct tissue-microstructure features. Magn Reson Med 60(2):439-448
20. Assaf Y, Freidlin RZ, Rohde GK, Basser PJ (2004) New modeling and experimental framework to characterize hindered and restricted water diffusion in brain white matter. Magn Reson Med 52(5):965-978 (Pubitemid 39453269)
21. Assaf Y, Blumenfeld-Katzir T, Yovel Y, Basser PJ (2008) AxCaliber: a method for measuring axon diameter distribution from diffusion MRI. Magn Reson Med 59(6):1347-1354 (Pubitemid 351813264)
22. Stanisz GJ, Szafer A, Wright GA, Henkelman M (1997) An analytical model of restricted diffusion in bovine optic nerve. Magn Reson Med 37:103-111 (Pubitemid 27008836)
23. Nilsson M, Lätt J, Nordh E, Wirestam R, Ståhlberg F, Brockstedt S (2009) On the effects of a varied diffusion time in vivo: is the diffusion in white matter restricted? Magn Reson Imaging 27(2):176-187
24. Basser PJ, Mattiello J, LeBihan D (1994) Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 103:247-254
25. Liu C, Bammer R, Acar B, Moseley ME (2004) Characterizing non-gaussian diffusion by using generalized diffusion tensors. Magn Reson Med 51(5):924-937 (Pubitemid 38580604)
26. Jensen JH, Helpern JA, Ramani A, Lu H, Kaczynski K (2005) Diffusional kurtosis imaging: the quantification of non-gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med 53(6):1432-1440 (Pubitemid 40734665)
27. Jensen JH, Helpern JA (2010) MRI quantification of non-gaussian water diffusion by kurtosis analysis. NMR Biomed 23(7):698-710
28. Bennett KM, Schmainda KM, Bennett RT, Rowe DB, Lu H, Hyde JS (2003) Characterization of continuously distributed cortical water diffusion rates with a stretched-exponential model. Magn Reson Med 50(4):727-734 (Pubitemid 37187837)
29. Yablonskiy DA, Bretthorst GL, Ackerman JJH (2003) Statistical model for diffusion attenuated MR signal. Magn Reson Med 50(4):664-669 (Pubitemid 37187828)
30. Fieremans E, Jensen JH, Helpern JA (2011) White matter characterization with diffusional kurtosis imaging. Neuroimage 58(1):177-188
31. Lätt J, Nilsson M, Rydhög A, Wirestam R, Ståhlberg F, Brockstedt S (2007) Effects of restricted diffusion in a biological phantom: a q-space diffusion MRI study of asparagus stems at a 3T clinical scanner. Magn Reson Mater Phy 20(4):213-222 (Pubitemid 350132161)
32. Lätt J, Nilsson M, Malmborg C, Rosquist H, Wirestam R, Ståhlberg F, Topgaard D, Brockstedt S (2007) Accuracy of q-space related parameters in MRI: simulations and phantom measurements. IEEE Trans Med Imaging 26(11):1437-1447 (Pubitemid 350025481)
33. Edgar JM, Griffiths IR (2009) White matter structure: a microscopist's view. In: Diffusion MRI from quantitative measurement to neuroanatomy, Academic Press, pp 73-103
34. Allen NJ, Barres BA (2009) Neuroscience: glia - more than just brain glue. Nature 457(7230):675-677
35. Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed 15(7-8):435-455 (Pubitemid 36054508)
36. Aboitiz F, Scheibel AB, Fisher RS, Zaidel E (1992) Fiber composition of the human corpus callosum. Brain Res 598(1-2):143-153 (Pubitemid 23013055)
37. Tang Y, Nyengaard JR, Pakkenberg B, Gundersen HJ (1997) Age-induced white matter changes in the human brain: a stereological investigation. Neurobiol Aging 18(6):609-615 (Pubitemid 28046413)
38. Michailov GV, Sereda MW, Brinkmann BG, Fischer TM, Haug B, Birchmeier C, Role L, Lai C, Schwab MH, Nave K-A (2004) Axonal neuregulin-1 regulates myelin sheath thickness. Science 304(5671):700-703 (Pubitemid 38560869)
39. Sturrock RR (1980) Myelination of the mouse corpus callosum. Neuropathol Appl Neurobiol 6(6):415-420 (Pubitemid 11215198)
40. Paus T (2010) Growth of white matter in the adolescent brain: myelin or axon? Brain Cognit 72(1):26-35
41. Waxman SG, Bennett MV (1972) Relative conduction velocities of small myelinated and non-myelinated fibres in the central nervous system. Nat New Biol 238(85):217-219
42. Rushton WAH (1951) A theory of the effects of fibre size in medullated nerve. J Physiol (Lond) 115(1):101-122
43. Hildebrand C, Remahl S, Persson H, Bjartmar C (1993) Myelinated nerve fibres in the CNS. Prog Neurobiol 40(3):319-384 (Pubitemid 23017425)
44. Hursh JB (1939) Conduction velocity and diameter of nerve fibers. Am J Physiol 127:131-139
45. Perge JA, Koch K, Miller R, Sterling P, Balasubramanian V (2009) How the optic nerve allocates space, energy capacity, and information. J Neurosci 29(24):7917-7928
46. Sunderland S (1965) The connective tissues of peripheral nerves. Brain 88(4):841-854
47. Breig A (1960) Biomechanics of the central nervous system: some basic normal and pathologic phenomena. Almqvist & Wiksell, Stockholm
48. Jeffery G (1996) PNS features of rodent optic nerve axons. J Comp Neurol 366(2):370-378 (Pubitemid 26070607)
49. Badaut J, Ashwal S, Adami A, Tone B, Recker R, Spagnoli D, Ternon B, Obenaus A (2011) Brain water mobility decreases after astrocytic aquaporin-4 inhibition using RNA interference. J Cereb Blood Flow Metab 31(3):819-831
50. Tait MJ, Saadoun S, Bell BA, Papadopoulos MC (2008) Water movements in the brain: role of aquaporins. Trends Neurosci 31(1):37-43
51. Castle NA (2005) Aquaporins as targets for drug discovery. Drug Discov Today 10(7):485-493
52. Clark CA, Le Bihan D (2000) Water diffusion compartmentation and anisotropy at high b values in the human brain. Magn Reson Med 44(6):852-859
53. Niendorf T, Dijkhuizen RM, Norris DG, van Lookeren Campagne M, Nicolay K (1996) Biexponential diffusion attenuation in various states of brain tissue: implications for diffusion-weighted imaging. Magn Reson Med 36(6):847-857 (Pubitemid 26396812)
54. Moseley ME, Cohen Y, Kucharczyk J, Mintorovitch J, Asgari HS, Wendland MF, Tsuruda J, Norman D (1990) Diffusion-weighted MR imaging of anisotropic water diffusion in cat central nervous system. Radiology 176(2):439-445 (Pubitemid 20225133)
55. Peled S (2007) New perspectives on the sources of white matter DTI signal. IEEE Trans Med Imaging 26(11):1448-1455 (Pubitemid 350025482)
56. Beaulieu C, Allen PS (1994) Water diffusion in the giant axon of the squid: implications for diffusion-weighted MRI of the nervous system. Magn Reson Med 32(5):579-583 (Pubitemid 24338205)
57. Beaulieu C, Allen PS (1996) An in vitro evaluation of the effects of local magnetic-susceptibility-induced gradients on anisotropic water diffusion in nerve. Magn Reson Med 36(1):39-44 (Pubitemid 26196529)
58. Frøhlich AF, Jespersen SN, Ostergaard L, Kiselev VG (2008) The effect of impermeable boundaries of arbitrary geometry on the apparent diffusion coefficient. J Magn Reson 194(1):128-135
59. Padhani AR, Liu G, Koh DM et al (2009) Diffusion-weighted magnetic resonance imaging as a cancer biomarker: consensus and recommendations. Neoplasia 11(2):102-125
60. Murday J, Cotts R (1968) Self-diffusion coefficient of liquid lithium. J Chem Phys 48:4938
61. Stepisnik J (1993) Time-dependent self-diffusion by NMR spin-echo. Phys B 183(4):343-350 (Pubitemid 23687884)
62. Neuman C (1974) Spin echo of spins diffusing in a bounded medium. J Chem Phys 60:4508
63. van Gelderen P, DesPres D, van Zijl PCM, Moonen CT (1994) Evaluation of restricted diffusion in cylinders. Phosphocreatine in rabbit leg muscle. J Magn Reson B 103(3):255-260
64. Wang L, Caprihan A, Fukushima E (1995) The narrow-pulse criterion for pulsed-gradient spin-echo diffusion measurements. J Magn Reson A 117(2):209-219
65. Zhang H, Barazany D, Assaf Y, Lundell HM, Alexander DC, Dyrby TB (2011) A comparative study of axon diameter imaging techniques using diffusion MRI. Proc Intl Soc Mag Reson Med 19:83
66. Cohen Y, Assaf Y (2002) High b-value q-space analyzed diffusion-weighted MRS and MRI in neuronal tissues - a technical review. NMR Biomed 15(7-8):516-542 (Pubitemid 36054513)
67. Alexander DC, Hubbard PL, Hall MG, Moore EA, Ptito M, Parker GJM, Dyrby TB (2010) Orientationally invariant indices of axon diameter and density from diffusion MRI. Neuroimage 52(4):1374-1389
68. Nilsson M, Alerstam E, Wirestam R, Ståhlberg F, Brockstedt S, Lätt J (2010) Evaluating the accuracy and precision of a two-compartment Kärger model using Monte Carlo simulations. J Magn Reson 206(1):59-67
69. Nilsson M, Alexander DC (2012) Investigating tissue microstructure using diffusion MRI: how does the resolution limit of the axon diameter relate to the maximal gradient strength? Proc Intl Soc Mag Reson Med 20:3567
70. Balinov B, Jonsson B, Linse P, Söderman O (1993) The NMR self-diffusion method applied to restricted diffusion. simulation of echo attenuation from molecules in spheres and between planes. J Magn Reson A 104(1):17-25
71. Callaghan P, Coy A, MacGowan D, Packer K, Zelaya F (1991) Diffraction-like effects in NMR diffusion studies of fluids in porous solids. Nature 351:467-469 (Pubitemid 21896618)
72. Avram L, Assaf Y, Cohen Y (2004) The effect of rotational angle and experimental parameters on the diffraction patterns and micro-structural information obtained from q-space diffusion NMR: implication for diffusion in white matter fibers. J Magn Reson 169(1):30-38
73. Avram L, Ozarslan E, Assaf Y, Bar-Shir A, Cohen Y, Basser PJ (2008) Three-dimensional water diffusion in impermeable cylindrical tubes: theory versus experiments. NMR Biomed 21(8):888-898
74. Lennon AJ, Kuchel PW (1994) Enhancement of the diffraction-like effect in NMR diffusion experiments. J Magn Reson A 111(2):208-211
75. Topgaard D, Söderman O (2003) Experimental determination of pore shape and size using q-space NMR microscopy in the long diffusion-time limit. Magn Reson Imaging 21(1):69-76 (Pubitemid 36293020)
76. Yablonskiy DA, Sukstanskii AL (2010) Theoretical models of the diffusion weighted MR signal. NMR Biomed 23(7):661-681
77. Peled S, Cory DG, Raymond SA, Kirschner DA, Jolesz FA (1999) Water diffusion, T(2), and compartmentation in frog sciatic nerve. Magn Reson Med 42(5):911-918 (Pubitemid 29521481)
78. Jespersen SN, Pedersen M, Stødkilde-Jørgensen H (2005) The influence of a cellular size distribution on NMR diffusion measurements. Eur Biophys J 34(7):890-898 (Pubitemid 41428186)
79. Leergaard TB, White NS, De Crespigny A, Bolstad I, D'arceuil H, Bjaalie JG, Dale AM (2010) Quantitative histological validation of diffusion MRI fiber orientation distributions in the rat brain. PLoS ONE 5(1):e8595
80. Nilsson M, Lätt J, Ståhlberg F, van Westen D, Hagslätt H (2012) The importance of axonal undulation in diffusion MR measurements: a Monte Carlo simulation study. NMR Biomed 25(5):795-805
81. Zhang H, Hubbard PL, Parker GJM, Alexander DC (2011) Axon diameter mapping in the presence of orientation dispersion with diffusion MRI. Neuroimage. doi: 10.1016/j.neuroimage.2011.01.084
82. Zhang H, Schneider T, Wheeler-Kingshott CA, Alexander DC (2012) NODDI: practical in vivo neurite orientation dispersion and density imaging of the human brain. Neuroimage 61(4):1000-1016
83. Karami G, Grundman N, Abolfathi N, Naik A, Ziejewski M (2009) A micromechanical hyperelastic modeling of brain white matter under large deformation. J Mech Behav Biomed Mater 2(3):243-254
84. Kärger J (1971) Der Einfluß der Zweibereichdiffusion auf die Spinechodämpfung unter Berücksichtigung der relaxation bei Messungen mit der Methode der gepulsten Feldgradienten. Ann Phys 482(1):107-109
85. Kärger J (1969) Zur Bestimmung der Diffusion in einem Zweibereichsystem mit Hilfe von gepulsten Feldgradienten. Ann Phys 479(1-2):1-4
86. Fieremans E, Novikov DS, Jensen JH, Helpern JA (2010) Monte Carlo study of a two-compartment exchange model of diffusion. NMR Biomed 23(7):711-724
87. Lasič S, Nilsson M, Lätt J, Ståhlberg F, Topgaard D (2011) Apparent exchange rate mapping with diffusion MRI. Magn Reson Med 66(2):356-365
88. Jansen M, Blume A (1995) A comparative study of diffusive and osmotic water permeation across bilayers composed of phospholipids with different head groups and fatty acyl chains. Biophys J 68(3):997-1008
89. Ye RG, Verkman AS (1989) Simultaneous optical measurement of osmotic and diffusional water permeability in cells and liposomes. Biochemistry 28(2):824-829 (Pubitemid 19047123)
90. Verkman AS (2000) Water permeability measurement in living cells and complex tissues. J Membr Biol 173(2):73-87 (Pubitemid 30051855)
91. Benga G (1988) Water transport in red blood cell membranes. Prog Biophys Mol Biol 51(3):193-245
92. Pfeuffer J, Flögel U, Dreher W, Leibfritz D (1998) Restricted diffusion and exchange of intracellular water: theoretical modelling and diffusion time dependence of 1H NMR measurements on perfused glial cells. NMR Biomed 11(1):19-31 (Pubitemid 28164845)
93. Meier C, Dreher W, Leibfritz D (2003) Diffusion in compartmental systems. I. A comparison of an analytical model with simulations. Magn Reson Med 50(3):500-509 (Pubitemid 37082074)
94. Lee J-H, Springer CS (2003) Effects of equilibrium exchange on diffusion-weighted NMR signals: the diffusigraphic "shutter-speed". Magn Reson Med 49(3):450-458 (Pubitemid 36262812)
95. Regan DG, Kuchel PW (2000) Mean residence time of molecules diffusing in a cell bounded by a semi-permeable membrane: Monte Carlo simulations and an expression relating membrane transition probability to permeability. Eur Biophys J 29:221-227
96. Sehy JV, Banks AA, Ackerman JJH, Neil JJ (2008) Importance of intracellular water apparent diffusion to the measurement of membrane permeability. Biophys J 83(5):2856-2863
97. Harkins KD, Galons J-P, Secomb TW, Trouard TP (2009) Assessment of the effects of cellular tissue properties on ADC measurements by numerical simulation of water diffusion. Magn Reson Med 62(6):1414-1422
98. Behrens TEJ, Berg HJ, Jbabdi S, Rushworth MFS, Woolrich MW (2007) Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage 34(1):144-155 (Pubitemid 44765263)
99. Jeurissen B, Leemans A, Tournier J-D, Jones DK, Sijbers J (2012) Investigating the prevalence of complex fiber configurations in white matter tissue with diffusion magnetic resonance imaging. Hum Brain Mapp. doi: 10.1002/hbm.22099
100. Lätt J, Nilsson M, Van Westen D, Wirestam R, Ståhlberg F, Brockstedt S (2009) Diffusion-weighted MRI measurements on stroke patients reveal water-exchange mechanisms in sub-acute ischaemic lesions. NMR Biomed 22(6):619-628
101. Kiselev VG, Il'yasov KA (2007) Is the "biexponential diffusion" biexponential? Magn Reson Med 57(3):464-469 (Pubitemid 46385855)
102. Panagiotaki E, Schneider T, Siow B, Hall MG, Lythgoe MF, Alexander DC (2012) Compartment models of the diffusion MR signal in brain white matter: a taxonomy and comparison. Neuroimage 59(3):2241-2254
103. Nilsson M, Lätt J, van Westen D, Brockstedt S, Lasič S, Ståhlberg F, Topgaard D (2012) Noninvasive mapping of water diffusional exchange in the human brain using filter-exchange imaging. Magn Reson Med. doi: 10.1002/mrm.24395
104. Nicholson C, Phillips JM (1981) Ion diffusion modified by tortuosity and volume fraction in the extracellular microenvironment of the rat cerebellum. J Physiol 321:225-257 (Pubitemid 12248093)
105. Lipinski H (1990) Monte Carlo simulation of extracellular diffusion in brain tissues. Phys Med Biol 35:441
106. Hall M, Alexander DC (2009) Convergence and parameter choice for Monte-Carlo simulations of diffusion MRI. IEEE Trans Med Imaging 28(9):1354-1364
107. Jin S, Zador Z, Verkman AS (2008) Random-walk model of diffusion in three dimensions in brain extracellular space: comparison with microfiberoptic photobleaching measurements. Biophys J 95(4):1785-1794
108. Jones DK, Cercignani M (2010) Twenty-five pitfalls in the analysis of diffusion MRI data. NMR Biomed 23(7):803-820
109. Le Bihan D, Poupon C, Amadon A, Lethimonnier F (2006) Artifacts and pitfalls in diffusion MRI. J Magn Reson Imaging 24(3):478-488 (Pubitemid 44320549)
110. Bernstein MA, Thomasson DM, Perman WH (1989) Improved detectability in low signal-to-noise ratio magnetic resonance images by means of a phase-corrected real reconstruction. Med Phys 16(5):813-817 (Pubitemid 19265742)
111. Gudbjartsson H, Patz S (1995) The Rician distribution of noisy MRI data. Magn Reson Med 34(6):910-914
112. Veraart J, Van Hecke W, Sijbers J (2011) Constrained maximum likelihood estimation of the diffusion kurtosis tensor using a Rician noise model. Magn Reson Med 66(3):678-686
113. Constantinides CD, Atalar E, McVeigh ER (1997) Signal-to-noise measurements in magnitude images from NMR phased arrays. Magn Reson Med 38(5):852-857 (Pubitemid 27467727)
114. Dietrich O, Raya JG, Reeder SB, Ingrisch M, Reiser MF, Schoenberg SO (2008) Influence of multichannel combination, parallel imaging and other reconstruction techniques on MRI noise characteristics. Magn Reson Imaging 26(6):754-762
115. Veraart J, Rajan J, Peeters RR, Leemans A, Sunaert S, Sijbers J (2012) Comprehensive framework for accurate diffusion MRI parameter estimation. Magn Reson Med. doi: 10.1002/mrm.24529
116. Pruessmann KP, Weiger M, Scheidegger MB, Boesiger P (1999) SENSE: sensitivity encoding for fast MRI. Magn Reson Med 42(5):952-962 (Pubitemid 29521486)
117. Thelwall PE, Shepherd TM, Stanisz GJ, Blackband SJ (2006) Effects of temperature and aldehyde fixation on tissue water diffusion properties, studied in an erythrocyte ghost tissue model. Magn Reson Med 56(2):282-289 (Pubitemid 44162775)
118. D'arceuil H, De Crespigny A (2007) The effects of brain tissue decomposition on diffusion tensor imaging and tractography. Neuroimage 36(1):64-68 (Pubitemid 46617946)
119. Sun S-W, Neil JJ, Liang H-F, He YY, Schmidt RE, Hsu CY, Song S-K (2005) Formalin fixation alters water diffusion coefficient magnitude but not anisotropy in infarcted brain. Magn Reson Med 53(6):1447-1451 (Pubitemid 40734667)
120. Schmierer K, Wheeler-Kingshott CAM, Tozer DJ, Boulby PA, Parkes HG, Yousry TA, Scaravilli F, Barker GJ, Tofts PS, Miller DH (2008) Quantitative magnetic resonance of postmortem multiple sclerosis brain before and after fixation. Magn Reson Med 59(2):268-277 (Pubitemid 351220090)
121. Dyrby TB, Baaré WFC, Alexander DC, Jelsing J, Garde E, Søgaard LV (2011) An ex vivo imaging pipeline for producing high-quality and high-resolution diffusion-weighted imaging datasets. Hum Brain Mapp 32(4):544-563
122. Andrasko J (1976) Water diffusion permeability of human erythrocytes studied by a pulsed gradient NMR technique. Biochim Biophys Acta 428(2):304-311
123. Thelwall PE, Grant SC, Stanisz GJ, Blackband SJ (2002) Human erythrocyte ghosts: exploring the origins of multiexponential water diffusion in a model biological tissue with magnetic resonance. Magn Reson Med 48(4):649-657
124. Benga G, Chapman BE, Kuchel PW (2009) Comparative NMR studies of diffusional water permeability of red blood cells from different species: XV. Agile wallaby (Macropus agilis), red-necked wallaby (Macropus rufogriseus) and Goodfellow's tree kangaroo (Dendrolagus goodfellowi). Comp Biochem Physiol A Physiol 154(1):105-109
125. Lisitza NV, Warren WS, Song Y-Q (2007) Study of diffusion in erythrocyte suspension using internal magnetic field inhomogeneity. J Magn Reson 187(1):146-154 (Pubitemid 46898876)
126. Zhao L, Sukstanskii AL, Kroenke CD, Song J, Piwnica-Worms D, Ackerman JJH, Niel JJ (2008) Intracellular Water Specific MR of Microbead-Adherent Cells: HeLa Cell Intracellular Water Diffusion. Magn Reson Med 59:79-84
127. Åslund I, Topgaard D (2009) Determination of the self-diffusion coefficient of intracellular water using PGSE NMR with variable gradient pulse length. J Magn Reson 201(2):250-254
128. Sehy JV, Ackerman JJH, Neil JJ (2002) Evidence that both fast and slow water ADC components arise from intracellular space. Magn Reson Med 48(5):765-770 (Pubitemid 35340316)
129. Galons J-P, Lope-Piedrafita S, Divijak JL, Corum C, Gillies RJ, Trouard TP (2005) Uncovering of intracellular water in cultured cells. Magn Reson Med 54(1):79-86 (Pubitemid 40898399)
130. Cooper RL, Chang DB, Young AC, Martin CJ, Ancker-Johnson D (1974) Restricted diffusion in biophysical systems. Experiment. Biophys J 14(3):161-177
131. Tanner JE (1979) Self diffusion of water in frog muscle. Biophys J 28(1):107-116 (Pubitemid 10204463)
132. Seo Y, Morita Y, Kusaka Y, Steward MC, Murakami M (1996) Diffusion of water in rat sciatic nerve measured by 1H pulsed field gradient NMR: compartmentation and anisotropy. Jpn J Physiol 46(2):163-169 (Pubitemid 26229277)
133. Assaf Y, Cohen Y (2000) Assignment of the water slow-diffusing component in the central nervous system using q-space diffusion MRS: implications for fiber tract imaging. Magn Reson Med 43(2):191-199 (Pubitemid 30075441)
134. Chin C-L, Wehrli FW, Fan Y, Hwang SN, Schwartz ED, Nissanov J, Hackney DB (2004) Assessment of axonal fiber tract architecture in excised rat spinal cord by localized NMR q-space imaging: simulations and experimental studies. Magn Reson Med 52(4):733-740 (Pubitemid 39314974)
135. Ong HH, Wright AC, Wehrli SL, Souza A, Schwartz ED, Hwang SN, Wehrli FW (2008) Indirect measurement of regional axon diameter in excised mouse spinal cord with q-space imaging: simulation and experimental studies. Neuroimage 40(4):1619-1632
136. Bar-Shir A, Cohen Y (2008) High b-value q-space diffusion MRS of nerves: structural information and comparison with histological evidence. NMR Biomed 21(2):165-174 (Pubitemid 351351009)
137. Biton IE, Duncan ID, Cohen Y (2007) q-Space diffusion of myelin-deficient spinal cords. Magn Reson Med 58(5):993-1000 (Pubitemid 350074367)
138. Ronen I, Moeller S, Ugurbil K, Kim D-S (2006) Analysis of the distribution of diffusion coefficients in cat brain at 9.4 T using the inverse Laplace transformation. Magn Reson Imaging 24(1):61-68 (Pubitemid 43061204)
139. Does MD, Beaulieu C, Allen PS, Snyder RE (1998) Multi-component T1 relaxation and magnetisation transfer in peripheral nerve. Magn Reson Imaging 16(9):1033-1041 (Pubitemid 29189660)
140. Beaulieu C, Fenrich FR, Allen PS (1998) Multicomponent water proton transverse relaxation and T2-discriminated water diffusion in myelinated and nonmyelinated nerve. Magn Reson Imaging 16(10):1201-1210 (Pubitemid 29019545)
141. Whittall KP, MacKay AL, Graeb DA, Nugent RA, Li DK, Paty DW (1997) In vivo measurement of T2 distributions and water contents in normal human brain. Magn Reson Med 37(1):34-43 (Pubitemid 27008828)
142. Laule C, Vavasour IM, Kolind SH, Li DKB, Traboulsee TL, Moore GRW, MacKay AL (2007) Magnetic resonance imaging of myelin. Neurotherapeutics 4(3):460-484 (Pubitemid 46962414)
143. Deoni SCL, Rutt BK, Arun T, Pierpaoli C, Jones DK (2008) Gleaning multicomponent T1 and T2 information from steady-state imaging data. Magn Reson Med 60(6):1372-1387
144. Does MD, Snyder RE (1995) T2 relaxation of peripheral nerve measured in vivo. Magn Reson Imaging 13(4):575-580
145. Mulkern RV, Zengingonul HP, Robertson RL et al (2000) Multi-component apparent diffusion coefficients in human brain: relationship to spin-lattice relaxation. Magn Reson Med 44(2):292-300 (Pubitemid 30614789)
146. Pfeuffer J, Provencher SW, Gruetter R (1999) Water diffusion in rat brain in vivo as detected at very large b values is multicompartmental. Magn Reson Mater Phy 8(2):98-108 (Pubitemid 29359854)
147. Huisman TAGM, Loenneker T, Barta G, Bellemann ME, Hennig J, Fischer JE, Il'yasov KA (2006) Quantitative diffusion tensor MR imaging of the brain: field strength related variance of apparent diffusion coefficient (ADC) and fractional anisotropy (FA) scalars. Eur Radiol 16(8):1651-1658 (Pubitemid 44027365)
148. Mulkern RV, Gudbjartsson H, Westin C-F et al (1999) Multi-component apparent diffusion coefficients in human brain. NMR Biomed 12(1):51-62 (Pubitemid 29135410)
149. Maier SE, Vajapeyam S, Mamata H, Westin C-F, Jolesz FA, Mulkern RV (2004) Biexponential diffusion tensor analysis of human brain diffusion data. Magn Reson Med 51(2):321-330 (Pubitemid 38173042)
150. Clark CA, Hedehus M, Moseley ME (2002) In vivo mapping of the fast and slow diffusion tensors in human brain. Magn Reson Med 47(4):623-628 (Pubitemid 34263773)
151. Syková E, Nicholson C (2008) Diffusion in brain extracellular space. Physiol Rev 88(4):1277-1340
152. Chin C-L, Wehrli FW, Hwang SN, Takahashi M, Hackney DB (2002) Biexponential diffusion attenuation in the rat spinal cord: computer simulations based on anatomic images of axonal architecture. Magn Reson Med 47(3):455-460 (Pubitemid 34193999)
153. Jespersen SN, Kroenke CD, Østergaard L, Ackerman JJH, Yablonskiy DA (2007) Modeling dendrite density from magnetic resonance diffusion measurements. Neuroimage 34(4):1473-1486 (Pubitemid 46187073)
154. Clark CA, Hedehus M, Moseley ME (2001) Diffusion time dependence of the apparent diffusion tensor in healthy human brain and white matter disease. Magn Reson Med 45(6):1126-1129 (Pubitemid 32488342)
155. Does MD, Parsons EC, Gore JC (2003) Oscillating gradient measurements of water diffusion in normal and globally ischemic rat brain. Magn Reson Med 49(2):206-215 (Pubitemid 36159856)
156. Jones DK (2003) Determining and visualizing uncertainty in estimates of fiber orientation from diffusion tensor MRI. Magn Reson Med 49(1):7-12 (Pubitemid 36042328)
157. Barazany D, Basser PJ, Assaf Y (2009) In vivo measurement of axon diameter distribution in the corpus callosum of rat brain. Brain 132(Pt 5):1210-1220
158. Quirk JD, Bretthorst GL, Duong TQ, Snyder AZ, Springer CS, Ackerman JJH, Neil JJ (2003) Equilibrium water exchange between the intra- and extracellular spaces of mammalian brain. Magn Reson Med 50(3):493-499 (Pubitemid 37082073)
159. Pfeuffer J, Bröer S, Bröer A, Lechte M, Flögel U, Leibfritz D (1998) Expression of aquaporins in Xenopus laevis oocytes and glial cells as detected by diffusion-weighted 1H NMR spectroscopy and photometric swelling assay. Biochim Biophys Acta 1448:27-36 (Pubitemid 28526616)
160. Does MD, Gore JC (2002) Compartmental study of T(1) and T(2) in rat brain and trigeminal nerve in vivo. Magn Reson Med 47(2):274-283 (Pubitemid 34116795)
161. Vavasour IM, Whittall KP, Li DK, MacKay AL (2000) Different magnetization transfer effects exhibited by the short and long T(2) components in human brain. Magn Reson Med 44(6):860-866
162. Ford JC, Hackney DB (1997) Numerical model for calculation of apparent diffusion coefficients (ADC) in permeable cylinders-comparison with measured ADC in spinal cord white matter. Magn Reson Med 37(3):387-394 (Pubitemid 27107964)
163. Hwang SN, Chin C-L, Wehrli FW, Hackney DB (2003) An image-based finite difference model for simulating restricted diffusion. Magn Reson Med 50(2):373-382 (Pubitemid 36950857)
164. Tien T, Ottova-Leitmannova A (2000) Membrane transport. In: Tien T, Ottova-Leitmannova A (eds) Membrane biophysics: as viewed from experimental bilayer lipid membranes (Planar lipid bilayers and spherical liposomes), 1st edn. Elsevier Science, Amsterdam, pp 221-282
165. Nilsson M, Hagslätt H, Van Westen D, Wirestam R, Ståhlberg F, Lätt J (2010) A mechanism for exchange between intraaxonal and extracellular water: Permeable nodes of Ranvier. Proc Intl Soc Mag Reson Med 18:1570
166. Sotak CH (2002) The role of diffusion tensor imaging in the evaluation of ischemic brain injury - a review. NMR Biomed 15(7-8):561-569 (Pubitemid 36054516)
167. Schwarcz A, Ursprung Z, Berente Z, Bogner P, Kotek G, Meric P, Gillet B, Beloeil J-C, Dóczi T (2007) In vivo brain edema classification: new insight offered by large b-value diffusion-weighted MR imaging. J Magn Reson Imaging 25(1):26-31 (Pubitemid 46098858)
168. Brugières P, Thomas P, Maraval A, Hosseini H, Combes C, Chafiq A, Ruel L, Breil S, Peschanski M, Gaston A (2004) Water diffusion compartmentation at high b values in ischemic human brain. Am J Neuroradiol 25(5):692-698 (Pubitemid 38657648)
169. Jensen JH, Falangola MF, Hu C, Tabesh A, Rapalino O, Lo C, Helpern JA (2011) Preliminary observations of increased diffusional kurtosis in human brain following recent cerebral infarction. NMR Biomed 24(5):452-457
170. Geijer B, Lindgren A, Brockstedt S, Ståhlberg F, Holtås S (2001) Persistent high signal on diffusion-weighted MRI in the late stages of small cortical and lacunar ischaemic lesions. Neuroradiology 43(2):115-122 (Pubitemid 32156700)
171. Yang Q, Tress BM, Barber PA, Desmond PM, Darby DG, Gerraty RP, Li T, Davis SM (1999) Serial study of apparent diffusion coefficient and anisotropy in patients with acute stroke. Stroke 30(11):2382-2390 (Pubitemid 29517739)
172. Budde MD, Frank JA (2010) Neurite beading is sufficient to decrease the apparent diffusion coefficient after ischemic stroke. Proc Natl Acad Sci USA 107(32):14472-14477
173. Does MD, Gore JC (2000) Compartmental study of diffusion and relaxation measured in vivo in normal and ischemic rat brain and trigeminal nerve. Magn Reson Med 43(6):837-844 (Pubitemid 30387604)
174. Silva MD, Omae T, Helmer KG, Li F, Fisher M, Sotak CH (2002) Separating changes in the intra- and extracellular water apparent diffusion coefficient following focal cerebral ischemia in the rat brain. Magn Reson Med 48(5):826-837 (Pubitemid 35340323)
175. Duong TQ, Ackerman JJH, Ying HS, Neil JJ (1998) Evaluation of extra- and intracellular apparent diffusion in normal and globally ischemic rat brain via 19F NMR. Magn Reson Med 40(1):1-13 (Pubitemid 28292579)
176. Sundgren PC, Dong Q, Gómez-Hassan D, Mukherji SK, Maly P, Welsh R (2004) Diffusion tensor imaging of the brain: review of clinical applications. Neuroradiology 46(5):339-350 (Pubitemid 38787262)
177. Sen PN, Basser PJ (2005) A model for diffusion in white matter in the brain. Biophys J 89(5):2927-2938 (Pubitemid 41636050)
178. Assaf Y, Pasternak O (2008) Diffusion tensor imaging (DTI)-based white matter mapping in brain research: a review. J Mol Neurosci 34(1):51-61 (Pubitemid 351378086)
179. Frank LR (2001) Anisotropy in high angular resolution diffusion-weighted MRI. Magn Reson Med 45(6):935-939 (Pubitemid 32488319)
180. Alexander AL, Hasan KM, Lazar M, Tsuruda JS, Parker DL (2001) Analysis of partial volume effects in diffusion-tensor MRI. Magn Reson Med 45(5):770-780 (Pubitemid 32402019)
181. Vos SB, Jones DK, Viergever MA, Leemans A (2011) Partial volume effect as a hidden covariate in DTI analyses. Neuroimage 55(4):1566-1576
182. Jones DK, Knösche TR, Turner R (2012) White matter integrity, fiber count, and other fallacies: the do's and don'ts of diffusion MRI. Neuroimage. doi: 10.1016/j.neuroimage.2012.06.081
183. Douaud G, Jbabdi S, Behrens TEJ et al (2011) DTI measures in crossing-fibre areas: increased diffusion anisotropy reveals early white matter alteration in MCI and mild Alzheimer's disease. Neuroimage 55(3):880-890
184. Tournier JD, Calamante F, Gadian DG, Connelly A (2004) Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution. Neuroimage 23(3):1176-1185 (Pubitemid 39446549)
185. Assaf Y, Ben-Bashat D, Chapman J et al (2002) High b-value q-space analyzed diffusion-weighted MRI: application to multiple sclerosis. Magn Reson Med 47(1):115-126 (Pubitemid 34019700)
186. Assaf Y, Mayzel-Oreg O, Gigi A et al (2002) High b value q-space-analyzed diffusion MRI in vascular dementia: a preliminary study. J Neurol Sci 203-204:235-239 (Pubitemid 35287404)
187. Mardor Y, Pfeffer R, Spiegelmann R et al (2003) Early detection of response to radiation therapy in patients with brain malignancies using conventional and high b-value diffusion-weighted magnetic resonance imaging. J Clin Oncol 21(6):1094-1100 (Pubitemid 46594139)
188. Van Essen DC, Ugurbil K, Auerbach E et al (2012) The human connectome project: a data acquisition perspective. Neuroimage 62(4):2222-2231
189. Schwarcz A, Bogner P, Meric P, Correze J-L, Berente Z, Pál J, Gallyas F, Doczi T, Gillet B, Beloeil J-C (2004) The existence of biexponential signal decay in magnetic resonance diffusion-weighted imaging appears to be independent of compartmentalization. Magn Reson Med 51(2):278-285 (Pubitemid 38168587)