In vivo high-resolution diffusion tensor imaging of the mouse brain

NeuroImage

Volumn 83, Issue , 2013, Pages 18-26

  Wu, Dan ^a   Xu, Jiadi ^b   McMahon, Michael T ^a,b   van Zijl, Peter C M ^a,b   Mori, Susumu ^a,b   Northington, Frances J ^a   Zhang, Jiangyang ^a  

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

^b KENNEDY KRIEGER INSTITUTE   (United States)

Author keywords

Brain atlas; Diffusion tensor imaging; High resolution; In vivo; Magnetic resonance imaging; Mouse brain

Indexed keywords

AMYGDALOID NUCLEUS; ANATOMICAL CONCEPTS; ANIMAL EXPERIMENT; ARTICLE; BRAIN TISSUE; CONTROLLED STUDY; CRYOPROBE; DIFFUSION TENSOR IMAGING; DIFFUSION WEIGHTED GRADIENT AND SPIN ECHO SEQUENCE; DIFFUSION WEIGHTED IMAGING; EX VIVO STUDY; FEMALE; HIGH RESOLUTION COMPUTER TOMOGRAPHY; HIPPOCAMPUS; HYPOTHALAMUS; IMAGE DISPLAY; IN VIVO STUDY; MORPHOLOGY; MOUSE; NEOCORTEX; NEUROANATOMY; NEUROIMAGING; NEWBORN; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; PRIORITY JOURNAL; STRUCTURE SEGMENTATION; THALAMUS; THREE DIMENSIONAL IMAGING; ANATOMIC MODEL; ANATOMY AND HISTOLOGY; ANIMAL; BIOLOGICAL MODEL; BRAIN; C57BL MOUSE; IMAGE ENHANCEMENT; IN VITRO STUDY; PROCEDURES; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY;

ANIMALS; ANIMALS, NEWBORN; BRAIN; DIFFUSION TENSOR IMAGING; FEMALE; IMAGE ENHANCEMENT; IMAGING, THREE-DIMENSIONAL; IN VITRO TECHNIQUES; MICE; MICE, INBRED C57BL; MODELS, ANATOMIC; MODELS, NEUROLOGICAL; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY;

EID: 84880933553     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.06.012     Document Type: Article

References (67)

1. Aggarwal M., Zhang J., Miller M.I., Sidman R.L., Mori S. Magnetic resonance imaging and micro-computed tomography combined atlas of developing and adult mouse brains for stereotaxic surgery. Neuroscience 2009, 162:1339-1350.
2. 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.
3. Aggarwal M., Duan W., Hou Z., Rakesh N., Peng Q., Ross C.A., Miller M.I., Mori S., Zhang J. Spatiotemporal mapping of brain atrophy in mouse models of Huntington's disease using longitudinal in vivo magnetic resonance imaging. Neuroimage 2012, 60:2086-2095.
4. Ali A.A., Dale A.M., Badea A., Johnson G.A. Automated segmentation of neuroanatomical structures in multispectral MR microscopy of the mouse brain. Neuroimage 2005, 27:425-435.
5. Badea A., Ali-Sharief A.A., Johnson G.A. Morphometric analysis of the C57BL/6J mouse brain. Neuroimage 2007, 37:683-693.
6. Baloch S., Verma R., Huang H., Khurd P., Clark S., Yarowsky P., Abel T., Mori S., Davatzikos C. Quantification of brain maturation and growth patterns in C57BL/6J mice via computational neuroanatomy of diffusion tensor images. Cereb. Cortex 2009, 19:675-687.
7. Baltes C., Radzwill N., Bosshard S., Marek D., Rudin M. Micro MRI of the mouse brain using a novel 400MHz cryogenic quadrature RF probe. NMR Biomed. 2009, 22:834-842.
8. Basser P.J., Mattiello J., LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophys. J. 1994, 66:259-267.
9. Benveniste H., Kim K., Zhang L., Johnson G.A. Magnetic resonance microscopy of the C57BL mouse brain. Neuroimage 2000, 11:601-611.
10. Bock N.A., Kovacevic N., Lipina T.V., Roder J.C., Ackerman S.L., Henkelman R.M. In vivo magnetic resonance imaging and semiautomated image analysis extend the brain phenotype for cdf/cdf mice. J. Neurosci. 2006, 26:4455-4459.
11. Budde M.D., Kim J.H., Liang H.F., Schmidt R.E., Russell J.H., Cross A.H., Song S.K. Toward accurate diagnosis of white matter pathology using diffusion tensor imaging. Magn. Reson. Med. 2007, 57:688-695.
12. Cahill L.S., Laliberte C.L., Ellegood J., Spring S., Gleave J.A., van Eede M.C., Lerch J.P., Henkelman R.M. Preparation of fixed mouse brains for MRI. Neuroimage 2012, 60:933-939.
13. Cai Y., McMurray M.S., Oguz I., Yuan H., Styner M.A., Lin W., Johns J.M., An H. Use of high resolution 3D diffusion tensor imaging to study brain white matter development in live neonatal rats. Front. Psychiatry 2011, 2:54.
14. Ceritoglu C., Oishi K., Li X., Chou M.C., Younes L., Albert M., Lyketsos C., van Zijl P.C., Miller M.I., Mori S. Multi-contrast large deformation diffeomorphic metric mapping for diffusion tensor imaging. Neuroimage 2009, 47:618-627.
15. Chahboune H., Ment L.R., Stewart W.B., Ma X., Rothman D.L., Hyder F. Neurodevelopment of C57B/L6 mouse brain assessed by in vivo diffusion tensor imaging. NMR Biomed. 2007, 20:375-382.
16. Chan E., Kovacevic N., Ho S.K., Henkelman R.M., Henderson J.T. Development of a high resolution three-dimensional surgical atlas of the murine head for strains 129S1/SvImJ and C57Bl/6J using magnetic resonance imaging and micro-computed tomography. Neuroscience 2007, 144:604-615.
17. Chuang N., Mori S., Yamamoto A., Jiang H., Ye X., Xu X., Richards L.J., Nathans J., Miller M.I., Toga A.W., Sidman R.L., Zhang J. An MRI-based atlas and database of the developing mouse brain. Neuroimage 2011, 54:80-89.
18. Conturo T.E., Lori N.F., Cull T.S., Akbudak E., Snyder A.Z., Shimony J.S., McKinstry R.C., Burton H., Raichle M.E. Tracking neuronal fiber pathways in the living human brain. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:10422-10427.
19. Dorr A.E., Lerch J.P., Spring S., Kabani N., Henkelman R.M. High resolution three-dimensional brain atlas using an average magnetic resonance image of 40 adult C57Bl/6J mice. Neuroimage 2008, 42:60-69.
20. Farrell J.A., Landman B.A., Jones C.K., Smith S.A., Prince J.L., van Zijl P.C., Mori S. Effects of signal-to-noise ratio on the accuracy and reproducibility of diffusion tensor imaging-derived fractional anisotropy, mean diffusivity, and principal eigenvector measurements at 1.5T. J. Magn. Reson. Imaging 2007, 26:756-767.
21. Farzaneh F., Riederer S.J., Pelc N.J. Analysis of T2 limitations and off-resonance effects on spatial resolution and artifacts in echo-planar imaging. Magn. Reson. Med. 1990, 14:123-139.
22. Flint J.J., Hansen B., Fey M., Schmidig D., King M.A., Vestergaard-Poulsen P., Blackband S.J. Cellular-level diffusion tensor microscopy and fiber tracking in mammalian nervous tissue with direct histological correlation. Neuroimage 2010, 52:556-561.
23. Gareis D., Wichmann T., Lanz T., MeIkus G., Horn M., Jakob P.M. Mouse MRI using phased-array coils. NMR Biomed. 2007, 20:326-334.
24. Harsan L.A., Paul D., Schnell S., Kreher B.W., Hennig J., Staiger J.F., von Elverfeldt D. In vivo diffusion tensor magnetic resonance imaging and fiber tracking of the mouse brain. NMR Biomed. 2010, 23:884-896.
25. Horsfield M.A., Jones D.K. Applications of diffusion-weighted and diffusion tensor MRI to white matter diseases - a review. NMR Biomed. 2002, 15:570-577.
26. Huang H., Zhang J., van Zijl P.C., Mori S. Analysis of noise effects on DTI-based tractography using the brute-force and multi-ROI approach. Magn. Reson. Med. 2004, 52:559-565.
27. Jacobs R.E., Ahrens E.T., Dickinson M.E., Laidlaw D. Towards a microMRI atlas of mouse development. Comput. Med. Imaging Graph. 1999, 23:15-24.
28. Jiang Y., Johnson G.A. Microscopic diffusion tensor imaging of the mouse brain. Neuroimage 2010, 50:465-471.
29. Jiang Y., Johnson G.A. Microscopic diffusion tensor atlas of the mouse brain. Neuroimage 2011, 56:1235-1243.
30. Jiang H., van Zijl P.C., Kim J., Pearlson G.D., Mori S. DtiStudio: resource program for diffusion tensor computation and fiber bundle tracking. Comput. Methods Programs Biomed. 2006, 81:106-116.
31. Kovacevic N., Henderson J.T., Chan E., Lifshitz N., Bishop J., Evans A.C., Henkelman R.M., Chen X.J. A three-dimensional MRI atlas of the mouse brain with estimates of the average and variability. Cereb. Cortex 2005, 15:639-645.
32. Landis J.R., Koch G.G. The measurement of observer agreement for categorical data. Biometrics 1977, 33:159-174.
33. Lau J.C., Lerch J.P., Sled J.G., Henkelman R.M., Evans A.C., Bedell B.J. Longitudinal neuroanatomical changes determined by deformation-based morphometry in a mouse model of Alzheimer's disease. Neuroimage 2008, 42:19-27.
34. Le Bihan D. Looking into the functional architecture of the brain with diffusion MRI. Nat. Rev. Neurosci. 2003, 4:469-480.
35. Lemke A., Heiler P., Stieltjes B., Neumann A., Schad L. High resolution in vivo DTI of the mouse brain: comparison of a cryogenic coil with a room temperature coil. The 18th annual meeting of the international society for magnetic resonance in medicine, Stockholm, Sweden 2010, 1700.
36. Lerch J.P., Carroll J.B., Spring S., Bertram L.N., Schwab C., Hayden M.R., Henkelman R.M. Automated deformation analysis in the YAC128 Huntington disease mouse model. Neuroimage 2008, 39:32-39.
37. Lori N.F., Akbudak E., Shimony J.S., Cull T.S., Snyder A.Z., Guillory R.K., Conturo T.E. Diffusion tensor fiber tracking of human brain connectivity: acquisition methods, reliability analysis and biological results. NMR Biomed. 2002, 15:494-515.
38. Ma Y., Hof P.R., Grant S.C., Blackband S.J., Bennett R., Slatest L., McGuigan M.D., Benveniste H. A three-dimensional digital atlas database of the adult C57BL/6J mouse brain by magnetic resonance microscopy. Neuroscience 2005, 135:1203-1215.
39. Ma Y., Smith D., Hof P.R., Foerster B., Hamilton S., Blackband S.J., Yu M., Benveniste H. In vivo 3D digital atlas database of the adult C57BL/6J mouse brain by magnetic resonance microscopy. Front. Neuroanat. 2008, 2:1.
40. Mac Donald C.L., Dikranian K., Bayly P., Holtzman D., Brody D. Diffusion tensor imaging reliably detects experimental traumatic axonal injury and indicates approximate time of injury. J. Neurosci. 2007, 27:11869-11876.
41. MacKenzie-Graham A., Lee E.F., Dinov I.D., Bota M., Shattuck D.W., Ruffins S., Yuan H., Konstantinidis F., Pitiot A., Ding Y., Hu G., Jacobs R.E., Toga A.W. A multimodal, multidimensional atlas of the C57BL/6J mouse brain. J. Anat. 2004, 204:93-102.
42. Mori S., van Zijl P.C. A motion correction scheme by twin-echo navigation for diffusion-weighted magnetic resonance imaging with multiple RF echo acquisition. Magn. Reson. Med. 1998, 40:511-516.
43. Mori S., van Zijl P.C. Fiber tracking: principles and strategies - a technical review. NMR Biomed. 2002, 15:468-480.
44. Mori S., Zhang J. Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 2006, 51:527-539.
45. Mori S., Crain B.J., Chacko V.P., van Zijl P.C. Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann. Neurol. 1999, 45:265-269.
46. Muller H.P., Vernikouskaya I., Ludolph A.C., Kassubek J., Rasche V. Fast diffusion tensor magnetic resonance imaging of the mouse brain at ultrahigh-field: aiming at cohort studies. PLoS One 2012, 7:e53389.
47. Natt O., Watanabe T., Boretius S., Radulovic J., Frahm J., Michaelis T. High-resolution 3D MRI of mouse brain reveals small cerebral structures in vivo. J. Neurosci. Methods 2002, 120:203-209.
48. Paxinos G., Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates 2003, Academic Press, Scan Diego. 2nd ed.
49. Paxinos G., Halliday G.M., Watson C., Koutcherov Y., Wang H. Atlas of the Developing Mouse Brain at E17.5, P0 and P6 2006, Academic Press, New York.
50. Petiet A.E., Kaufman M.H., Goddeeris M.M., Brandenburg J., Elmore S.A., Johnson G.A. High-resolution magnetic resonance histology of the embryonic and neonatal mouse: a 4D atlas and morphologic database. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:12331-12336.
51. Pierpaoli C., Basser P.J. Toward a quantitative assessment of diffusion anisotropy. Magn. Reson. Med. 1996, 36:893-906.
52. Ratering D., Baltes C., Nordmeyer-Massner J., Marek D., Rudin M. Performance of a 200-MHz cryogenic RF probe designed for MRI and MRS of the murine brain. Magn. Reson. Med. 2008, 59:1440-1447.
53. Ren T., Zhang J., Plachez C., Mori S., Richards L.J. Diffusion tensor magnetic resonance imaging and tract-tracing analysis of Probst bundle structure in Netrin1- and DCC-deficient mice. J. Neurosci. 2007, 27:10345-10349.
54. Sawiak S.J., Wood N.I., Williams G.B., Morton A.J., Carpenter T.A. Voxel-based morphometry in the R6/2 transgenic mouse reveals differences between genotypes not seen with manual 2D morphometry. Neurobiol. Dis. 2009, 33:20-27.
55. Shepherd T.M., Thelwall P.E., Stanisz G.J., Blackband S.J. Aldehyde fixative solutions alter the water relaxation and diffusion properties of nervous tissue. Magn. Reson. Med. 2009, 62:26-34.
56. Sun S.W., Neil J.J., Liang H.F., He Y.Y., Schmidt R.E., Hsu C.Y., Song S.K. Formalin fixation alters water diffusion coefficient magnitude but not anisotropy in infarcted brain. Magn. Reson. Med. 2005, 53:1447-1451.
57. Sun S.W., Liang H.F., Trinkaus K., Cross A.H., Armstrong R.C., Song S.K. Noninvasive detection of cuprizone induced axonal damage and demyelination in the mouse corpus callosum. Magn. Reson. Med. 2006, 55:302-308.
58. Sun S.W., Liang H.F., Xie M., Oyoyo U., Lee A. Fixation, not death, reduces sensitivity of DTI in detecting optic nerve damage. Neuroimage 2009, 44:611-619.
59. Tannus A., Garwood M. Adiabatic pulses. NMR Biomed. 1997, 10:423-434.
60. Toga A.W., Thompson P.M. Temporal dynamics of brain anatomy. Annu. Rev. Biomed. Eng. 2003, 5:119-145.
61. Tyszka J.M., Readhead C., Bearer E.L., Pautler R.G., Jacobs R.E. Statistical diffusion tensor histology reveals regional dysmyelination effects in the shiverer mouse mutant. Neuroimage 2006, 29:1058-1065.
62. Wang S., Wu E.X., Tam C.N., Lau H.F., Cheung P.T., Khong P.L. Characterization of white matter injury in a hypoxic-ischemic neonatal rat model by diffusion tensor MRI. Stroke 2008, 39:2348-2353.
63. Wang S., Wu E.X., Cai K., Lau H.F., Cheung P.T., Khong P.L. Mild hypoxic-ischemic injury in the neonatal rat brain: longitudinal evaluation of white matter using diffusion tensor MR imaging. AJNR Am. J. Neuroradiol. 2009, 30:1907-1913.
64. Woods R.P., Grafton S.T., Watson J.D., Sicotte N.L., Mazziotta J.C. Automated image registration: II. Intersubject validation of linear and nonlinear models. J. Comput. Assist. Tomogr. 1998, 22:153-165.
65. Zhang J., Richards L.J., Yarowsky P., Huang H., van Zijl P.C., Mori S. Three-dimensional anatomical characterization of the developing mouse brain by diffusion tensor microimaging. Neuroimage 2003, 20:1639-1648.
66. Zhang J., Peng Q., Li Q., Jahanshad N., Hou Z., Jiang M., Masuda N., Langbehn D.R., Miller M.I., Mori S., Ross C.A., Duan W. Longitudinal characterization of brain atrophy of a Huntington's disease mouse model by automated morphological analyses of magnetic resonance images. Neuroimage 2010, 49:2340-2351.
67. Zhang J., Jones M.V., McMahon M.T., Mori S., Calabresi P.A. In vivo and ex vivo diffusion tensor imaging of cuprizone-induced demyelination in the mouse corpus callosum. Magn. Reson. Med. 2011, 67:750-759.