In vivo and ex vivo diffusion tensor imaging of cuprizone-induced demyelination in the mouse corpus callosum

Magnetic Resonance in Medicine

Volumn 67, Issue 3, 2012, Pages 750-759

  Zhang, Jiangyang ^a   Jones, Melina V ^a   McMahon, Michael T ^b   Mori, Susumu ^a,b   Calabresi, Peter A ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KENNEDY KRIEGER INSTITUTE   (United States)

Author keywords

cuprizone; demyelination; diffusion tensor imaging; diffusivity; mouse brain

Indexed keywords

ANISOTROPY; CLUSTERING ALGORITHMS; DIFFUSION; MAGNETIC RESONANCE IMAGING; PATHOLOGY; TENSORS;

CUPRIZONE; DEMYELINATION; DIFFUSIVITY MEASUREMENTS; FRACTIONAL ANISOTROPY; IN-VIVO MEASUREMENT; MOUSE BRAIN; POTENTIAL CHANGE; TISSUE MICROSTRUCTURES;

DIFFUSION TENSOR IMAGING;

CUPRIZONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AXONAL INJURY; C57BL 6 MOUSE; CONTROLLED STUDY; CORPUS CALLOSUM; DEMYELINATION; DIFFUSION TENSOR IMAGING; EX VIVO STUDY; FEMALE; FRACTIONAL ANISOTROPY; IN VIVO STUDY; MOUSE; NONHUMAN; PATHOLOGY;

EID: 84857365918     PISSN: 07403194     EISSN: 15222594     Source Type: Journal    
DOI: 10.1002/mrm.23032     Document Type: Article

References (40)

1. Basser PJ, Mattiello J, LeBihan D,. MR diffusion tensor spectroscopy and imaging. Biophys J 1994; 66: 259-267. (Pubitemid 24016507)
2. Le Bihan D,. Looking into the functional architecture of the brain with diffusion MRI. Nat Rev Neurosci 2003; 4: 469-480. (Pubitemid 37280168)
3. Mori S, Zhang J,. Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 2006; 51: 527-539. (Pubitemid 44301829)
4. Basser P, Pierpaoli C,. Microstructural and physiological features of tissues elucidated by quantitative-dfifusion-tensor MRI. J Magn Reson B 1996; 111: 209-219. (Pubitemid 126758682)
5. Neil J, Miller J, Mukherjee P, Huppi PS,. Diffusion tensor imaging of normal and injured developing human brainâa technical review. NMR Biomed 2002; 15: 543-552. (Pubitemid 36054514)
6. Pierpaoli C, Barnett A, Pajevic S, Chen R, Penix LR, Virta A, Basser P,. Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. Neuroimage 2001; 13 (6 Pt 1): 1174-1185. (Pubitemid 32553548)
7. Horsfield MA, Jones DK,. Applications of diffusion-weighted and diffusion tensor MRI to white matter diseasesâa review. NMR Biomed 2002; 15: 570-577. (Pubitemid 36054517)
8. Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH,. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 2002; 17: 1429-1436. (Pubitemid 35333862)
9. Song SK, Sun SW, Ju WK, Lin SJ, Cross AH, Neufeld AH,. Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage 2003; 20: 1714-1722. (Pubitemid 37468277)
10. 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. J Neurosci 2009; 29: 2805-2813.
11. DeBoy CA, Zhang J, Dike S, Shats I, Jones M, Reich DS, Mori S, Nguyen T, Rothstein B, Miller RH, Griffin JT, Kerr DA, Calabresi PA,. High resolution diffusion tensor imaging of axonal damage in focal inflammatory and demyelinating lesions in rat spinal cord. Brain 2007; 130 (Pt 8): 2199-2210. (Pubitemid 47236617)
12. Shepherd TM, Thelwall PE, Stanisz GJ, Blackband SJ,. Aldehyde fixative solutions alter the water relaxation and diffusion properties of nervous tissue. Magn Reson Med 2009; 62: 26-34.
13. Sun SW, Neil JJ, Song SK,. Relative indices of water diffusion anisotropy are equivalent in live and formalin-fixed mouse brains. Magn Reson Med 2003; 50: 743-748. (Pubitemid 37187839)
14. Pattany PM, Puckett WR, Klose KJ, Quencer RM, Bunge RP, Kasuboski L, Weaver RG,. High-resolution diffusion-weighted MR of fresh and fixed cat spinal cords: evaluation of diffusion coefficients and anisotropy. AJNR Am J Neuroradiol 1997; 18: 1049-1056. (Pubitemid 30412126)
15. D'Arceuil HE, Westmoreland S, de Crespigny AJ,. An approach to high resolution diffusion tensor imaging in fixed primate brain. Neuroimage 2007; 35: 553-565. (Pubitemid 46402978)
16. Guilfoyle DN, Helpern JA, Lim KO,. Diffusion tensor imaging in fixed brain tissue at 7.0 T. NMR Biomed 2003; 16: 77-81. (Pubitemid 36582226)
17. Matsushima GK, Morell P,. The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathol 2001; 11: 107-116.
18. Stidworthy MF, Genoud S, Suter U, Mantei N, Franklin RJ,. Quantifying the early stages of remyelination following cuprizone-induced demyelination. Brain Pathol 2003; 13: 329-339. (Pubitemid 36975823)
19. Smith BR, Huff DS, Johnson GA,. Magnetic resonance imaging of embryos: an internet resource for the study of embryonic development. Comput Med Imaging Graph 1999; 23: 33-40. (Pubitemid 29159806)
20. Benveniste H, Blackband S,. MR microscopy and high resolution small animal MRI: applications in neuroscience research. Prog Neurobiol 2002; 67: 393-420. (Pubitemid 35257912)
21. Aggarwal M, Mori S, Shimogori T, Blackshaw S, Zhang J,. Three-dimensional diffusion tensor microimaging for anatomical characterization of the mouse brain. Magn Reson Med 2010; 64: 249-261.
22. Jiang H, van Zijl PC, Kim J, Pearlson GD, Mori S,. DtiStudio: resource program for diffusion tensor computation and fiber bundle tracking. Comput Methods Programs Biomed 2006; 81: 106-116. (Pubitemid 43144442)
23. Woods RP, Grafton ST, Holmes CJ, Cherry SR, Mazziotta JC,. Automated image registration: I. General methods and intrasubject, intramodality validation. J Comput Assist Tomogr 1998; 22: 139-152. (Pubitemid 28087337)
24. Woods RP, Grafton ST, Watson JD, Sicotte NL, Mazziotta JC,. Automated image registration: II. Intersubject validation of linear and nonlinear models. J Comput Assist Tomogr 1998; 22: 153-165. (Pubitemid 28087338)
25. Xu D, Mori S, Shen D, van Zijl PC, Davatzikos C,. Spatial normalization of diffusion tensor fields. Magn Reson Med 2003; 50: 175-182. (Pubitemid 36841873)
26. Zhang J, Jones M, DeBoy CA, Reich DS, Farrell JA, Hoffman PN, Griffin JW, Sheikh KA, Miller MI, Mori S, Calabresi PA,. Diffusion tensor magnetic resonance imaging of Wallerian degeneration in rat spinal cord after dorsal root axotomy. J Neurosci 2009; 29: 3160-3171.
27. Xie M, Tobin JE, Budde MD, Chen CI, Trinkaus K, Cross AH, McDaniel DP, Song SK, Armstrong RC,. Rostrocaudal analysis of corpus callosum demyelination and axon damage across disease stages refines diffusion tensor imaging correlations with pathological features. J Neuropathol Exp Neurol 2010; 69: 704-716.
28. Kipp M, Clarner T, Dang J, Copray S, Beyer C,. The cuprizone animal model: new insights into an old story. Acta Neuropathol 2009; 118: 723-736.
29. Liu L, Belkadi A, Darnall L, Hu T, Drescher C, Cotleur AC, Padovani-Claudio D, He T, Choi K, Lane TE, Miller RH, Ransohoff RM,. CXCR2-positive neutrophils are essential for cuprizone-induced demyelination: relevance to multiple sclerosis. Nat Neurosci 2010; 13: 319-326.
30. Carlton WW,. Studies on the induction of hydrocephalus and spongy degeneration by cuprizone feeding and attempts to antidote the toxicity. Life Sci 1967; 6: 11-19.
31. Harsan LA, Steibel J, Zaremba A, Agin A, Sapin R, Poulet P, Guignard B, Parizel N, Grucker D, Boehm N, Miller RH, Ghandour MS,. Recovery from chronic demyelination by thyroid hormone therapy: myelinogenesis induction and assessment by diffusion tensor magnetic resonance imaging. J Neurosci 2008; 28: 14189-14201.
32. Merkler D, Boretius S, Stadelmann C, Ernsting T, Michaelis T, Frahm J, Bruck W,. Multicontrast MRI of remyelination in the central nervous system. NMR Biomed 2005; 18: 395-403. (Pubitemid 41410360)
33. Zaaraoui W, Deloire M, Merle M, Girard C, Raffard G, Biran M, Inglese M, Petry KG, Gonen O, Brochet B, Franconi JM, Dousset V,. Monitoring demyelination and remyelination by magnetization transfer imaging in the mouse brain at 9.4 T. MAGMA 2008; 21: 357-362.
34. Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, Armstrong RC,. Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 2005; 26: 132-140. (Pubitemid 40602893)
35. Sun SW, Liang HF, Trinkaus K, Cross AH, Armstrong RC, Song SK,. Noninvasive detection of cuprizone induced axonal damage and demyelination in the mouse corpus callosum. Magn Reson Med 2006; 55: 302-308. (Pubitemid 43238098)
36. Sun SW, Neil JJ, Liang HF, He YY, Schmidt RE, Hsu CY, Song SK,. Formalin fixation alters water diffusion coefficient magnitude but not anisotropy in infarcted brain. Magn Reson Med 2005; 53: 1447-1451. (Pubitemid 40734667)
37. Beaulieu C,. The basis of anisotropic water diffusion in the nervous systemâa technical review. NMR Biomed 2002; 15: 435-455. (Pubitemid 36054508)
38. Shepherd TM, Flint JJ, Thelwall PE, Stanisz GJ, Mareci TH, Yachnis AT, Blackband SJ,. Postmortem interval alters the water relaxation and diffusion properties of rat nervous tissueâimplications for MRI studies of human autopsy samples. Neuroimage 2009; 44: 820-826.
39. Boonstra H, Oosterhuis JW, Oosterhuis AM, Fleuren GJ,. Cervical tissue shrinkage by formaldehyde fixation, paraffin wax embedding, section cutting and mounting. Virchows Arch A Pathol Anat Histopathol 1983; 402: 195-201. (Pubitemid 14208545)
40. Quester R, Schroder R,. The shrinkage of the human brain stem during formalin fixation and embedding in paraffin. J Neurosci Methods 1997; 75: 81-89. (Pubitemid 27314531)