Cited by 117Advanced Neuroimaging Techniques and ApplicationsAdvanced MRI Techniques and ApplicationsNMR spectroscopy and applications

Probing mouse brain microstructure using oscillating gradient diffusion MRI

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Aggarwal, Manisha, Jones, Melina V., Calabresi, Peter A., Mori, Susumu, Zhang, Jiangyang·2012·Magnetic Resonance in Medicine

Abstract

High resolution diffusion tensor images of the mouse brain were acquired using the pulsed gradient spin echo sequence and the oscillating gradient spin echo sequence. The oscillating gradient spin echo tensor images demonstrated frequency‐dependent changes in diffusion measurements, including apparent diffusion coefficient and fractional anisotropy, in major brain structures. Maps of the rate of change in apparent diffusion coefficient with oscillating gradient frequency revealed novel tissue contrast in the mouse hippocampus, cerebellum, and cerebral cortex. The observed frequency‐dependent contrasts resembled neuronal soma‐specific Nissl staining and nuclei‐specific 4′,6‐diamidino‐2‐phenylindole (DAPI) staining in the mouse brain, which suggests that the contrasts might be related to key features of cytoarchitecture in the brain. In the mouse cuprizone model, oscillating gradient spin echo‐based diffusion MRI revealed significantly higher frequency‐dependence of perpendicular diffusivity (λ ⊥ ) in the demyelinated caudal corpus callosum at 4 weeks after cuprizone treatment when compared with control mice and mice at 6 weeks after cuprizone treatment. The elevated frequency‐dependence of λ ⊥ coincided with the infiltration of activated microglia/macrophages and disruption of axons during acute demyelination in the caudal corpus callosum. The results demonstrate the potential of oscillating gradient spin echo‐based diffusion MRI for providing tissue contrasts complimentary to conventional pulsed gradient spin echo‐based diffusion MRI. Magn Reson Med 67:98–109, 2012. © 2011 Wiley Periodicals, Inc.

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  • Demyelinated areas have extensive infiltration and amplification of cells that distort the normal tissue structure in the acute demyelination cuprizone model.

    “It’s reported that demyelinated areas have extensive infiltration and amplification of cells that distort the normal tissue structure in acute demyelination cuprizone model (Aggarwal et al. 2012; Sun et al. 2006).”

    From Neurite orientation dispersion and density imaging of mouse brain microstructure (2019) · cites this paper as Aggarwal et al. 2012

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References 50 · Cited by 117

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  1. [1]Chenevert TL McKeever PE Ross BD Monitoring early response of experimental brain tumors to therapy using diffusion magnetic resonance imaging Clin Cancer Res 1997 3 9 1457 1466 9815831
  2. [2]Moffat BA Chenevert TL Lawrence TS Meyer CR Johnson TD Dong Q Tsien C Mukherji S Quint DJ Gebarski SS Robertson PL Junck LR Rehemtulla A Ross BD Functional diffusion map: a noninvasive MRI biomarker for early stratification of clinical brain tumor response Proc Natl Acad Sci U S A 2005 102 15 5524 5529 15805192 PMC555936
  3. [3]Moseley ME Cohen Y Mintorovitch J Chileuitt L Shimizu H Kucharczyk J Wendland MF Weinstein PR Early detection of regional cerebral ischemia in cats: comparison of diffusion- and T2-weighted MRI and spectroscopy Magn Reson Med 1990 14 2 330 346 2345513
  4. [4]Cercignani M Bozzali M Iannucci G Comi G Filippi M Magnetisation transfer ratio and mean diffusivity of normal appearing white and grey matter from patients with multiple sclerosis J Neurol Neurosurg Psychiatry 2001 70 3 311 317 11181851 PMC1737283
  5. [5]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 11352623
  6. [6]Le Bihan D Looking into the functional architecture of the brain with diffusion MRI Nat Rev Neurosci 2003 4 6 469 480 12778119
  7. [7]Basser P Pierpaoli C Microstructural and physiological features of tissues elucidated by quantitative-dfifusion-tensor MRI J Magn Reson B 1996 111 209 219 8661285
  8. [8]Mori S Zhang J Principles of diffusion tensor imaging and its applications to basic neuroscience research Neuron 2006 51 5 527 539 16950152
  9. [9]Callagan PT Principles of Nuclear Magnetic Resonance Microscopy 1991 Oxford University Press New York
  10. [11]Kim S Chi-Fishman G Barnett AS Pierpaoli C Dependence on diffusion time of apparent diffusion tensor of ex vivo calf tongue and heart Magn Reson Med 2005 54 6 1387 1396 16265644
  11. [12]Latour LL Svoboda K Mitra PP Sotak CH Time-dependent diffusion of water in a biological model system Proc Natl Acad Sci U S A 1994 91 4 1229 1233 8108392 PMC43130
  12. [13]Niendorf T Norris DG Leibfritz D Detection of apparent restricted diffusion in healthy rat brain at short diffusion times Magn Reson Med 1994 32 5 672 677 7808271
  13. [14]Ozarslan E Basser PJ Shepherd TM Thelwall PE Vemuri BC Blackband SJ Observation of anomalous diffusion in excised tissue by characterizing the diffusion-time dependence of the MR signal J Magn Reson 2006 183 2 315 323 16962801
  14. [17]Parsons EC Does MD Gore JC Modified oscillating gradient pulses for direct sampling of the diffusion spectrum suitable for imaging sequences Magn Reson Imaging 2003 21 3-4 279 285 12850719
  15. [18]Schachter M Does MD Anderson AW Gore JC Measurements of restricted diffusion using an oscillating gradient spin-echo sequence J Magn Reson 2000 147 2 232 237 11097814
  16. [21]Parsons EC Jr. Does MD Gore JC Temporal diffusion spectroscopy: theory and implementation in restricted systems using oscillating gradients Magn Reson Med 2006 55 1 75 84 16342147
  17. [22]Gore JC Xu J Colvin DC Yankeelov TE Parsons EC Does MD Characterization of tissue structure at varying length scales using temporal diffusion spectroscopy NMR Biomed 2010 23 7 745 756 20677208 PMC3285511
  18. [23]Colvin DC Yankeelov TE Does MD Yue Z Quarles C Gore JC New insights into tumor microstructure using temporal diffusion spectroscopy Cancer Res 2008 68 14 5941 5947 18632649 PMC2719758
  19. [24]Does MD Parsons EC Gore JC Oscillating gradient measurements of water diffusion in normal and globally ischemic rat brain Magn Reson Med 2003 49 2 206 215 12541239
  20. [26]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 1 33 40 10091866
  21. [27]Benveniste H Blackband S MR microscopy and high resolution small animal MRI: applications in neuroscience research Prog Neurobiol 2002 67 5 393 420 12234501
  22. [28]Xu J Does MD Gore JC Sensitivity of MR diffusion measurements to variations in intracellular structure: effects of nuclear size Magn Reson Med 2009 61 4 828 833 19205020 PMC2749035
  23. [29]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 1 249 261 20577980 PMC2915547
  24. [30]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 2 106 116 16413083
  25. [31]Baschong W Suetterlin R Laeng RH Control of autofluorescence of archival formaldehyde-fixed, paraffin-embedded tissue in confocal laser scanning microscopy (CLSM) J Histochem Cytochem 2001 49 12 1565 1572 11724904
  26. [32]Paxinos G Franklin K The Mouse Brain in Stereotaxic Coordinates: Compact 2003 Academic Press Second Edition
  27. [33]Stepisnik J Callaghan PT Low-frequency velocity correlation spectrum of fluid in a porous media by modulated gradient spin echo Magn Reson Imaging 2001 19 3-4 469 472 11445332
  28. [34]Stepisnik J Lasic S Mohoric A Sersa I Sepe A Spectral characterization of diffusion in porous media by the modulated gradient spin echo with CPMG sequence J Magn Reson 2006 182 2 195 199 16844392
  29. [35]Paxinos G The Rat Nervous System 2004 Academic Press New York
  30. [36]Zhao C Teng EM Summers RG Jr. Ming GL Gage FH Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus J Neurosci 2006 26 1 3 11 16399667 PMC6674324
  31. [37]Diaz-Cintra S Yong A Aguilar A Bi X Lynch G Ribak CE Ultrastructural analysis of hippocampal pyramidal neurons from apolipoprotein E-deficient mice treated with a cathepsin inhibitor J Neurocytol 2004 33 1 37 48 15173631
  32. [38]Kim SU Observations on cerebellar granule cells in tissue culture. A silver and electron microscopic study Z Zellforsch Mikrosk Anat 1970 107 4 454 465 5448478
  33. [39]Wimer RE Wimer CC A biometrical-genetic analysis of granule cell number in the area dentata of house mice Brain Res 1981 254 1 129 140 7272765
  34. [40]Wimer RE Wimer CC Chernow CR Balvanz BA The genetic organization of neuron number in the pyramidal cell layer of hippocampal regio superior in house mice Brain Res 1980 196 1 59 77 7397531
  35. [41]Stidworthy MF Genoud S Suter U Mantei N Franklin RJ Quantifying the early stages of remyelination following cuprizone-induced demyelination Brain Pathol 2003 13 3 329 339 12946022 PMC8095752
  36. [42]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 1 132 140 15862213
  37. [43]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 2 302 308 16408263
  38. [44]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 69 7 704 716 20535036 PMC2901930
  39. [45]Pfeuffer J Flogel U Dreher W Leibfritz D Restricted diffusion and exchange of intracellular water: theoretical modelling and diffusion time dependence of 1H NMR measurements on perfused glial cells NMR Biomed 1998 11 1 19 31 9608585
  40. [46]Clark CA Le Bihan D Water diffusion compartmentation and anisotropy at high b values in the human brain Magn Reson Med 2000 44 6 852 859 11108621
  41. [47]Thelwall PE Shepherd TM Stanisz GJ Blackband SJ Effects of temperature and aldehyde fixation on tissue water diffusion properties, studied in an erythrocyte ghost tissue model Magn Reson Med 2006 56 2 282 289 16841346
  42. [49]Xu J Does MD Gore JC Quantitative characterization of tissue microstructure with temporal diffusion spectroscopy J Magn Reson 2009 200 2 189 197 19616979 PMC2758625

Authors
Aggarwal, M., Jones, M. V., Calabresi, P. A., Mori, S., & Zhang, J.
Affiliations
  • Johns Hopkins University (US)
  • Kennedy Krieger Institute (US)
Corresponding author
Zhang, Jiangyang
Venue
Magnetic Resonance in Medicine
Publisher
Wiley
Published
2011-05-16
Volume
67
Issue
1
Pages
98-109
ISSN
  • 0740-3194 (ISSN-L)
  • 1522-2594
OpenAlex
W2103939073
Cited by
117
References
50
Citations by year
2026: 4 · 2025: 7 · 2024: 9 · 2023: 9 · 2022: 10 · 2021: 8 · 2020: 15 · 2019: 9 · 2018: 10 · 2017: 3 · 2016: 7 · 2015: 7 · 2014: 8 · 2013: 6 · 2012: 5
FWCI
4.61
Type
journal article
Language
en
Open access
Locations
  • Magnetic Resonance in Medicine (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • Multiple Sclerosis Society
  • National Institute on Aging (R01AG020012)
  • National Institute of Neurological Disorders and Stroke (R01NS070909, R21NS065306, R21NS059529)
  • National Institute of Biomedical Imaging and Bioengineering (R01EB003543)
Topics
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
  • Physical Sciences › Physics and Astronomy › Nuclear and High Energy Physics › NMR spectroscopy and applications
Keywords
oscillating gradient spin echo, diffusion MRI, apparent diffusion coefficient, fractional anisotropy, cuprizone demyelination, corpus callosum, hippocampus, cerebellum, cerebral cortex, cytoarchitecture, microglia/macrophage infiltration, axonal disruption, Nissl staining, DAPI staining
MeSH terms
Algorithms, Animals, Brain, Female, Image Enhancement, Image Interpretation, Computer-Assisted, Mice, Inbred C57BL, Oscillometry, Sensitivity and Specificity, Reproducibility of Results, Diffusion Magnetic Resonance Imaging, Mice

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