Unveiling early cortical and subcortical neuronal degeneration in ALS mice by ultra-high field diffusion MRI

References

• Wijesekera LC, Leigh PN. Amyotrophic lateral sclerosis. Orphanet J Rare Dis. 2009;4:3.
   PubMed Web of Science ®Google Scholar
• Abdulla S, Machts J, Kaufmann J, Patrick K, Kollewe K, Dengler R, et al. Hippocampal degeneration in patients with amyotrophic lateral sclerosis. Neurobiol Aging. 2014;35:2639–45.
   PubMed Web of Science ®Google Scholar
• Ferrari R, Kapogiannis D, Huey ED, Momeni P. FTD and ALS: a tale of two diseases. Car. 2011;8:273–94.
   Google Scholar
• Phukan J, Elamin M, Bede P, Jordan N, Gallagher L, Byrne S, et al. The syndrome of cognitive impairment in amyotrophic lateral sclerosis: a population-based study. J Neurol Neurosurg Psychiatry. 2012;83:102–8.
   PubMed Web of Science ®Google Scholar
• Tsermentseli S, Leigh PN, Goldstein LH. The anatomy of cognitive impairment in amyotrophic lateral sclerosis: more than frontal lobe dysfunction. Cortex. 2012;48:166–82.
   PubMed Web of Science ®Google Scholar
• Agosta F, Valsasina P, Riva N, Copetti M, Messina MJ, Prelle A, et al. The cortical signature of amyotrophic lateral sclerosis. PLoS One. 2012;7:e42816.
   PubMed Web of Science ®Google Scholar
• Raaphorst J, van Tol MJ, de Visser M, van der Kooi AJ, Majoie CB, van den Berg LH, et al. Prose memory impairment in amyotrophic lateral sclerosis patients is related to hippocampus volume. Eur J Neurol. 2015;22:547–54.
   PubMed Web of Science ®Google Scholar
• Agosta F, Chio A, Cosottini M, De Stefano N, Falini A, Mascalchi M, et al. The present and the future of neuroimaging in amyotrophic lateral sclerosis. AJNR Am J Neuroradiol. 2010;31:1769–77.
   PubMed Web of Science ®Google Scholar
• Borsodi F, Culea V, Langkammer C, Khalil M, Pirpamer L, Quasthoff S, et al. Multimodal assessment of white matter tracts in amyotrophic lateral sclerosis. PloS One. 2017;12:e0178371.
   PubMed Web of Science ®Google Scholar
• Gatto RG, Chauhan M, Chauhan N. Anti-edema effects of rhEpo in experimental traumatic brain injury. Rnn. 2015;33:927–41.
   Google Scholar
• Baldaranov D, Khomenko A, Kobor I, Bogdahn U, Gorges M, Kassubek J, et al. Longitudinal diffusion tensor imaging-based assessment of tract alterations: an application to amyotrophic lateral sclerosis. Front Hum Neurosci. 2017;11:567.
   PubMed Web of Science ®Google Scholar
• Broad RJ, Gabel MC, Dowell NG, Schwartzman DJ, Seth AK, Zhang H, et al. Neurite orientation and dispersion density imaging (NODDI) detects cortical and corticospinal tract degeneration in ALS. J Neurol Neurosurg Psychiatry. 2019;90:404–411.
   Web of Science ®Google Scholar
• Gatto RG, Amin MY, Deyoung D, Hey M, Mareci TH, Magin RL. Ultra-high field diffusion MRI reveals early axonal pathology in spinal cord of ALS mice. Transl Neurodegener. 2018;7:20.
   PubMed Web of Science ®Google Scholar
• Cohen-Adad J, Zhao W, Keil B, Ratai EM, Triantafyllou C, Lawson R, et al. 7-T MRI of the spinal cord can detect lateral corticospinal tract abnormality in amyotrophic lateral sclerosis. Muscle Nerve. 2013;47:760–2.
   PubMed Web of Science ®Google Scholar
• Heiman-Patterson TD, Deitch JS, Blankenhorn EP, Erwin KL, Perreault MJ, Alexander BK, et al. Background and gender effects on survival in the TgN(SOD1-G93A)1Gur mouse model of ALS. J Neurol Sci. 2005;236:1–7.
   PubMed Web of Science ®Google Scholar
• Gatto RG, Chu Y, Ye AQ, Price SD, Tavassoli E, Buenaventura A, et al. Analysis of YFP(J16)-R6/2 reporter mice and postmortem brains reveals early pathology and increased vulnerability of callosal axons in Huntington's disease. Hum Mol Genet. 2015;24:5285–98.
   PubMed Web of Science ®Google Scholar
• Yushkevich PA, Yang G, Gerig G. ITK-SNAP: An interactive tool for semi-automatic segmentation of multi-modality biomedical images. Conference proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society IEEE Engineering in Medicine and Biology Society Annual Conference, Orlando, FL, USA, August 16–20, 2016;3342–5.
   Google Scholar
• Paxinos G, Franklin KBJ. The mouse brain in stereotaxic coordinates. Compact 2nd ed. Amsterdam; Boston: Elsevier Academic Press; 2004.
   Google Scholar
• Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM. Fsl. Neuroimage. 2012;62:782–90.
   PubMed Web of Science ®Google Scholar
• Kodiweera C, Alexander AL, Harezlak J, McAllister TW, Wu YC. Age effects and sex differences in human brain white matter of young to middle-aged adults: a DTI, NODDI, and q-space study. NeuroImage. 2016;128:180–92.
   PubMed Web of Science ®Google Scholar
• Tabesh A, Jensen JH, Ardekani BA, Helpern JA. Estimation of tensors and tensor-derived measures in diffusional kurtosis imaging. Magn Reson Med. 2011;65:823–36.
   PubMed Web of Science ®Google Scholar
• Lu H, Jensen JH, Ramani A, Helpern JA. Three-dimensional characterization of non-gaussian water diffusion in humans using diffusion kurtosis imaging. NMR Biomed. 2006;19:236–47.
   PubMed Web of Science ®Google Scholar
• Gatto RG, Mustafi SM, Amin MY, Mareci TH, Wu YC, Magin RL. Neurite orientation dispersion and density imaging can detect presymptomatic axonal degeneration in the spinal cord of ALS mice. Funct Neurol. 2018;33:155–63.
   PubMed Web of Science ®Google Scholar
• Gatto RG, Ye AQ, Colon-Perez L, Mareci TH, Lysakowski A, Price SD, et al. Detection of axonal degeneration in a mouse model of Huntington’s disease: comparison between diffusion tensor imaging and anomalous diffusion metrics. Magnet Reson Mat Phys Biol Med. 2019. doi:10.1007/s10334-019-00742-6.
   Web of Science ®Google Scholar
• Bede P, Bokde AL, Byrne S, Elamin M, McLaughlin RL, Kenna K, et al. Multiparametric MRI study of ALS stratified for the C9orf72 genotype. Neurology. 2013;81:361–9.
   PubMed Web of Science ®Google Scholar
• 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;29:2805–13.
   PubMed Web of Science ®Google Scholar
• 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;55:302–8.
   PubMed Web of Science ®Google Scholar
• 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;17:1429–36.
   PubMed Web of Science ®Google Scholar
• Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, et al. Demyelination increases radial diffusivity in corpus callosum of mouse brain. NeuroImage. 2005;26:132–40.
   PubMed Web of Science ®Google Scholar
• Gatto RG, Li W, Gao J, Magin RL. In vivo diffusion MRI detects early spinal cord axonal pathology in a mouse model of amyotrophic lateral sclerosis. NMR Biomed. 2018;31:e3954.
   PubMed Web of Science ®Google Scholar
• Fischer LR, Culver DG, Tennant P, Davis AA, Wang M, Castellano-Sanchez A, et al. Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp Neurol. 2004;185:232–40.
   PubMed Web of Science ®Google Scholar
• Genc B, Jara JH, Lagrimas AK, Pytel P, Roos RP, Mesulam MM, et al. Apical dendrite degeneration, a novel cellular pathology for Betz cells in ALS. Sci Rep. 2017;7, 41765. doi:10.1038/srep41765.
   Web of Science ®Google Scholar
• Ozdinler PH, Benn S, Yamamoto TH, Guzel M, Brown RH, Jr, Macklis JD. Corticospinal motor neurons and related subcerebral projection neurons undergo early and specific neurodegeneration in hSOD1G(9)(3)A transgenic ALS mice. J Neurosci. 2011;31:4166–77.
   PubMed Web of Science ®Google Scholar
• Meadowcroft MD, Mutic NJ, Bigler DC, Wang JL, Simmons Z, Connor JR, et al. Histological-MRI correlation in the primary motor cortex of patients with amyotrophic lateral sclerosis. J Magn Reson Imaging. 2015;41:665–75.
   PubMed Web of Science ®Google Scholar
• Machts J, Loewe K, Kaufmann J, Jakubiczka S, Abdulla S, Petri S, et al. Basal ganglia pathology in ALS is associated with neuropsychological deficits. Neurology. 2015;85:1301–9.
   PubMed Web of Science ®Google Scholar
• Bede P, Elamin M, Byrne S, McLaughlin RL, Kenna K, Vajda A, et al. Basal ganglia involvement in amyotrophic lateral sclerosis. Neurology. 2013;81:2107–15.
   PubMed Web of Science ®Google Scholar
• Westeneng HJ, Verstraete E, Walhout R, Schmidt R, Hendrikse J, Veldink JH, et al. Subcortical structures in amyotrophic lateral sclerosis. Neurobiol Aging. 2015;36:1075–82.
   PubMed Web of Science ®Google Scholar
• d'Ambrosio A, Gallo A, Trojsi F, Corbo D, Esposito F, Cirillo M, et al. Frontotemporal cortical thinning in amyotrophic lateral sclerosis. AJNR Am J Neuroradiol. 2014;35:304–10.
   PubMed Web of Science ®Google Scholar
• Grosskreutz J, Kaufmann J, Fradrich J, Dengler R, Heinze HJ, Peschel T. Widespread sensorimotor and frontal cortical atrophy in Amyotrophic Lateral Sclerosis. BMC Neurol. 2006;6:17.
   PubMed Web of Science ®Google Scholar
• Hansen B, Jespersen SN. Kurtosis fractional anisotropy, its contrast and estimation by proxy. Sci Rep. 2016;6, 23999. doi:10.1038/srep23999.
   Web of Science ®Google Scholar
• Magin RL, Ingo C, Colon-Perez L, Triplett W, Mareci TH. Characterization of anomalous diffusion in porous biological tissues using fractional order derivatives and entropy. Microporous Mesoporous Mater. 2013;178:39–43.
   PubMed Web of Science ®Google Scholar
• Devine MS, Pannek K, Coulthard A, McCombe PA, Rose SE, Henderson RD. Exposing asymmetric gray matter vulnerability in amyotrophic lateral sclerosis. NeuroImage Clin. 2015;7:782–7.
   PubMed Web of Science ®Google Scholar
• Jones DK, Knosche TR, Turner R. White matter integrity, fiber count, and other fallacies: the do's and don'ts of diffusion MRI. NeuroImage. 2013;73:239–54.
   PubMed Web of Science ®Google Scholar
• Schilling K, Gao Y, Janve V, Stepniewska I, Landman BA, Anderson AW. Can increased spatial resolution solve the crossing fiber problem for diffusion MRI? NMR Biomed. 2017;30:e3787. doi:10.1002/nbm.3787.
   Web of Science ®Google Scholar
• Roebroeck A, Miller KL, Aggarwal M. Ex vivo diffusion MRI of the human brain: technical challenges and recent advances. NMR Biomed. 2018;32:e3941.
   PubMed Web of Science ®Google Scholar
• Stanton BR, Shinhmar D, Turner MR, Williams VC, Williams SC, Blain CR, et al. Diffusion tensor imaging in sporadic and familial (D90A SOD1) forms of amyotrophic lateral sclerosis. Arch Neurol. 2009;66:109–15.
   PubMed Web of Science ®Google Scholar
• Blain CR, Brunton S, Williams VC, Leemans A, Turner MR, Andersen PM, et al. Differential corticospinal tract degeneration in homozygous 'D90A' SOD-1 ALS and sporadic ALS. J Neurol Neurosurg Psychiatry. 2011;82:843–9.
   PubMed Web of Science ®Google Scholar
• Turner MR, Hammers A, Al-Chalabi A, Shaw CE, Andersen PM, Brooks DJ, et al. Distinct cerebral lesions in sporadic and 'D90A' SOD1 ALS: studies with [11C]flumazenil PET. Brain. 2005;128:1323–9.
   PubMed Web of Science ®Google Scholar
• Turner MR, Hammers A, Allsop J, Al-Chalabi A, Shaw CE, Brooks DJ, et al. Volumetric cortical loss in sporadic and familial amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2007;8:343–7.
   PubMed Web of Science ®Google Scholar