Magnetic resonance imaging of pathological processes in rodent models of amyotrophic lateral sclerosis

References

• Rothstein JD. Current hypotheses for the underlying bio-logy of amyotrophic lateral sclerosis. Ann Neurol. 2009;65(Suppl 1):S3–9.
   PubMed Web of Science ®Google Scholar
• Turner MR, Kiernan MC, Leigh PN, Talbot K. Biomarkers in amyotrophic lateral sclerosis. Lancet Neurol. 2009;8:94–109.
   PubMed Web of Science ®Google Scholar
• Turner MR, Modo M. Advances in the application of MRI to amyotrophic lateral sclerosis. Expert Opinion on Medical Diagnostics. 2010;4:483–96.
   PubMedGoogle Scholar
• Gurney ME. Transgenic mouse model of amyotrophic lateral sclerosis. N Engl J Med. 1994;331:1721–2.
   PubMed Web of Science ®Google Scholar
• Turner BJ, Talbot K. Transgenics, toxicity and therapeutics in rodent models of mutant SOD1-mediated familial ALS. Prog Neurobiol. 2008;85:94–134.
   PubMed Web of Science ®Google Scholar
• van den Bosch L. Genetic rodent models of amyotrophic lateral sclerosis. J Biomed Biotechnol. 2011epub;2011:348765.
   PubMedGoogle Scholar
• Benatar M. Lost in translation: treatment trials in the SOD1 mouse and in human ALS. Neurobiol Dis. 2007;26:1–13.
   PubMed Web of Science ®Google Scholar
• Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, . Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science. 2006;314:130–3.
   PubMed Web of Science ®Google Scholar
• Miller MW, Chiaia NL, Rhoades RW. Intracellular recording and injection study of corticospinal neurons in the rat somatosensory cortex: effect of prenatal exposure to ethanol. J Comp Neurol. 1990;297:91–105.
   PubMed Web of Science ®Google Scholar
• Lemon RN. Descending pathways in motor control. Annu Rev Neurosci. 2008;31:195–218.
   PubMed Web of Science ®Google Scholar
• Terashima T. Anatomy, development and lesion-induced plasticity of rodent corticospinal tract. Neurosci Res. 1995;22:139–61.
   PubMedGoogle Scholar
• Bortoff GA, Strick PL. Corticospinal terminations in two New-World primates: further evidence that corticomotoneuronal connections provide part of the neural substrate for manual dexterity. J Neurosci. 1993;13:5105–18.
   PubMedGoogle Scholar
• Kuypers HG. The Descending Pathways to the Spinal Cord, Their Anatomy and Function. Prog Brain Res. 1964;11:178–202.
   PubMedGoogle Scholar
• Lemon R. The output map of the primate motor cortex. Trends Neurosci. 1988;11:501–6.
   PubMedGoogle Scholar
• Porter S, Glaser L, Bunge RP. Release of autocrine growth factor by primary and immortalized Schwann cells. Proc Natl Acad Sci U S A. 1987;84:7768–72.
   PubMedGoogle Scholar
• Alstermark B, Ogawa J. In vivo recordings of bulbospinal excitation in adult mouse forelimb motor neurons. J Neurophysiol. 2004;92:1958–62.
   PubMedGoogle Scholar
• Alstermark B, Ogawa J, Isa T. Lack of monosynaptic corticomotoneuronal EPSPs in rats: disynaptic EPSPs mediated via reticulospinal neurons and polysynaptic EPSPs via segmental interneurons. J Neurophysiol. 2004;91:1832–9.
   PubMed Web of Science ®Google Scholar
• Illert M, Lundberg A, Tanaka R. Integration in descending motor pathways controlling the forelimb in the cat. 1. Pyramidal effects on motor neurons. Exp Brain Res. 1976;26:509–19.
   PubMed Web of Science ®Google Scholar
• Valverde F. The pyramidal tract in rodents. A study of its relations with the posterior column nuclei, dorsolateral reticular formation of the medulla oblongata, and cervical spinal cord (Golgi and electron microscopic observations). Z Zellforsch Mikrosk Anat. 1966;71:298–363.
   PubMedGoogle Scholar
• Babalian A, Liang F, Rouiller EM. Cortical influences on cervical motor neurons in the rat: recordings of synaptic responses from motor neurons and compound action potential from corticospinal axons. Neurosci Res. 1993;16:301–10.
   PubMedGoogle Scholar
• Gemma M, Perego GB, Pizzini G, Tredici G. Distribution of the corticospinal fibres in the cervical and lumbar enlargements of the rat spinal cord. Journal Fur Hirnforschung. 1987;28:457–62.
   PubMedGoogle Scholar
• Massion J. Red nucleus: past and future. Behav Brain Res. 1988;28:1–8.
   PubMedGoogle Scholar
• Ruigrok TGH, Cella F. Precerebellar nuclei and red nucleus. In: Paxinos G, editor. The Rat Nervous System. 2ndedn. New York: Academic Press; 1995.277–308.
   Google Scholar
• Whishaw IQ, Gorny B, Sarna J. Paw and limb use in skilled and spontaneous reaching after pyramidal tract, red nucleus and combined lesions in the rat: behavioural and anatomical dissociations. Behav Brain Res. 1998;93:167–83.
   PubMed Web of Science ®Google Scholar
• Siklos L, Engelhardt JI, Alexianu ME, Gurney ME, Siddique T, Appel SH. Intracellular calcium parallels motor neuron degeneration in SOD-1 mutant mice. J Neuropathol Exp Neurol. 1998;57:571–87.
   PubMed Web of Science ®Google Scholar
• Bruijn LI, Houseweart MK, Kato S, Anderson KL, Anderson SD, Ohama E, . Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science. 1998;281:1851–4.
   PubMed Web of Science ®Google Scholar
• Wang J, Slunt H, Gonzales V, Fromholt D, Coonfield M, Copeland NG, . Copper-binding-site-null SOD1 causes ALS in transgenic mice: aggregates of non-native SOD1 delineate a common feature. Hum Mol Genet. 2003;12:2753–64.
   PubMed Web of Science ®Google Scholar
• Mackenzie IR, Bigio EH, Ince PG, Geser F, Neumann M, Cairns NJ, . Pathological TDP-43 distinguishes sporadic amyotrophic lateral sclerosis from amyotrophic lateral sclerosis with SOD1 mutations. Ann Neurol. 2007;61:427–34.
   PubMed Web of Science ®Google Scholar
• Turner BJ, Baumer D, Parkinson NJ, Scaber J, Ansorge O, Talbot K. TDP-43 expression in mouse models of amyotrophic lateral sclerosis and spinal muscular atrophy. BMC Neurosci. 2008;9:104.
   PubMed Web of Science ®Google Scholar
• Wegorzewska I, Baloh RH. TDP-43-Based Animal Models of Neurodegeneration: New Insights into ALS Pathology and Pathophysiology. Neurodegener Dis. 2011;8:262–74.
   PubMed Web of Science ®Google Scholar
• Chang JL, Lomen-Hoerth C, Murphy J, Henry RG, Kramer JH, Miller BL, . A voxel-based morphometry study of patterns of brain atrophy in ALS and ALS/FTLD. Neurology. 2005;65:75–80.
   PubMed Web of Science ®Google Scholar
• Kassubek J, Unrath A, Huppertz HJ, Lule D, Ethofer T, Sperfeld AD, . Global brain atrophy and corticospinal tract alterations in ALS, as investigated by voxel-based morphometry of 3-D MRI. Amyotroph Lateral Scler Other Motor Neuron Disord. 2005;6:213–20.
   PubMed Web of Science ®Google Scholar
• Chen Z, Ma L. Grey matter volume changes over the whole brain in amyotrophic lateral sclerosis: A voxel-wise meta-analysis of voxel based morphometry studies. Amyotroph Lateral Scler. 2010 epub;11:549–54.
   PubMed Web of Science ®Google Scholar
• Petrik MS, Wilson JM, Grant SC, Blackband SJ, Tabata RC, Shan X, . Magnetic resonance microscopy and immunohistochemistry of the CNS of the mutant SOD murine model of ALS reveals widespread neural deficits. Neuromolecular Med. 2007;9:216–29.
   PubMed Web of Science ®Google Scholar
• Wilson JM, Petrik MS, Grant SC, Blackband SJ, Lai J, Shaw CA. Quantitative measurement of neurodegeneration in an ALS-PDC model using MR microscopy. Neuroimage. 2004;23:336–43.
   PubMedGoogle Scholar
• Brooks KJ, Hill MD, Hockings PD, Reid DG. MRI detects early hindlimb muscle atrophy in Gly93Ala superoxide dismutase-1 (G93A-SOD1) transgenic mice: an animal model of familial amyotrophic lateral sclerosis. NMR Biomed. 2004;17:28–32.
   PubMed Web of Science ®Google Scholar
• Helpern JA, Lee SP, Falangola MF, Dyakin VV, Bogart A, Ardekani B, . MRI assessment of neuropathology in a transgenic mouse model of Alzheimer's disease. Magn Reson Med. 2004;51:794–8.
   PubMed Web of Science ®Google Scholar
• Angenstein F, Niessen HG, Goldschmidt J, Vielhaber S, Ludolph AC, Scheich H. Age-dependent changes in MRI of motor brain stem nuclei in a mouse model of ALS. Neuroreport. 2004;15:2271–4.
   PubMed Web of Science ®Google Scholar
• Niessen HG, Angenstein F, Sander K, Kunz WS, Teuchert M, Ludolph AC, . In vivo quantification of spinal and bulbar motor neuron degeneration in the G93A-SOD1 transgenic mouse model of ALS by T2 relaxation time and apparent diffusion coefficient. Exp Neurol. 2006;201:293–300.
   PubMed Web of Science ®Google Scholar
• Zang DW, Yang Q, Wang HX, Egan G, Lopes EC, Cheema SS. Magnetic resonance imaging reveals neuronal degeneration in the brainstem of the superoxide dismutase-1 transgenic mouse model of amyotrophic lateral sclerosis. Eur J Neurosci. 2004;20:1745–51.
   PubMed Web of Science ®Google Scholar
• Ellis CM, Simmons A, Dawson JM, Williams SC, Leigh PN. Distinct hyperintense MRI signal changes in the corticospinal tracts of a patient with motor neuron disease. Amyotroph Lateral Scler Other Motor Neuron Disord. 1999;1:41–4.
   PubMedGoogle Scholar
• Waragai M. MRI and clinical features in amyotrophic lateral sclerosis. Neuroradiology. 1997;39:847–51.
   PubMed Web of Science ®Google Scholar
• Benveniste H, Einstein G, Kim KR, Hulette C, Johnson GA. Detection of neuritic plaques in Alzheimer's disease by magnetic resonance microscopy. Proc Natl Acad Sci U S A. 1999;96:14079–84.
   PubMedGoogle Scholar
• Falangola MF, Lee SP, Nixon RA, Duff K, Helpern JA. Histological colocalization of iron in Abeta plaques of PS/APP transgenic mice. Neurochem Res. 2005;30:201–5.
   PubMedGoogle Scholar
• Langkammer C, Enzinger C, Quasthoff S, Grafenauer P, Soellinger M, Fazekas F, . Mapping of iron deposition in conjunction with assessment of nerve fibre tract integrity in amyotrophic lateral sclerosis. J Magn Reson Imaging. 2010;31:1339–45.
   PubMed Web of Science ®Google Scholar
• Bucher S, Braunstein KE, Niessen HG, Kaulisch T, Neumaier M, Boeckers TM, . Vacuolization correlates with spin-spin relaxation time in motor brainstem nuclei and behavioural tests in the transgenic G93A-SOD1 mouse model of ALS. Eur J Neurosci. 2007;26:1895–901.
   PubMedGoogle Scholar
• Higgins CMJ, Jung CW, Xu ZS. ALS-associated mutant SOD1-G93A causes mitochondrial vacuolation by expansion of the intermembrane space and by involvement of SOD1 aggregation and peroxisomes. BMC Neuroscience. 2003;4:7–16.
   PubMedGoogle Scholar
• Kong JM, Xu ZS. Massive mitochondrial degeneration in motor neurons triggers the onset of amyotrophic lateral sclerosis in mice expressing a mutant SOD1. Journal of Neuroscience. 1998;18:3241–50.
   PubMed Web of Science ®Google Scholar
• Jaarsma D, Haasdijk ED, Grashorn JA, Hawkins R, van Duijn W, Verspaget HW, . Human Cu/Zn superoxide dismutase (SOD1) overexpression in mice causes mitochondrial vacuolization, axonal degeneration, and premature motor neuron death and accelerates motor neuron disease in mice expressing a familial amyotrophic lateral sclerosis mutant SOD1. Neurobiol Dis. 2000;7:623–43.
   PubMed Web of Science ®Google Scholar
• Mattiazzi M, D'Aurelio M, Gajewski CD, Martushova K, Kiaei M, Beal MF, . Mutated human SOD1 causes dysfunction of oxidative phosphorylation in mitochondria of transgenic mice. Journal of Biological Chemistry. 2002;277:29626–33.
   PubMed Web of Science ®Google Scholar
• Peretti-Viton P, Azulay JP, Trefouret S, Brunel H, Daniel C, Viton JM, . MRI of the intracranial corticospinal tracts in amyotrophic and primary lateral sclerosis. Neuroradiology. 1999;41:744–9.
   PubMed Web of Science ®Google Scholar
• Andreassen OA, Jenkins BG, Dedeoglu A, Ferrante KL, Bogdanov MB, Kaddurah-Daouk R, . Increases in cortical glutamate concentrations in transgenic amyotrophic lateral sclerosis mice are attenuated by creatine supplementation. J Neurochem. 2001;77:383–90.
   PubMed Web of Science ®Google Scholar
• Niessen HG, Debska-Vielhaber G, Sander K, Angenstein F, Ludolph AC, Hilfert L, . Metabolic progression markers of neurodegeneration in the transgenic G93A-SOD1 mouse model of amyotrophic lateral sclerosis. Eur J Neurosci. 2007;25:1669–77.
   PubMed Web of Science ®Google Scholar
• Pioro EP, Wang Y, Moore JK, Ng TC, Trapp BD, Klinkosz B, . Neuronal pathology in the Wobbler mouse brain revealed by in vivo proton magnetic resonance spectroscopy and immunocytochemistry. Neuroreport. 1998;9:3041–6.
   PubMedGoogle Scholar
• von Kienlin M, Kunnecke B, Metzger F, Steiner G, Richards JG, Ozmen L, . Altered metabolic profile in the frontal cortex of PS2APP transgenic mice, monitored throughout their life span. Neurobiol Dis. 2005;18:32–9.
   PubMed Web of Science ®Google Scholar
• Dedeoglu A, Choi JK, Cormier K, Kowall NW, Jenkins BG. Magnetic resonance spectroscopic analysis of Alzheimer's disease mouse brain that expresses mutant human APP shows altered neurochemical profile. Brain Res. 2004;1012:60–5.
   PubMed Web of Science ®Google Scholar
• Broom KA, Anthony DC, Lowe JP, Griffin JL, Scott H, Blamire AM, . MRI and MRS alterations in the preclinical phase of murine prion disease: association with neuropathological and behavioural changes. Neurobiol Dis. 2007;26:707–17.
   PubMed Web of Science ®Google Scholar
• Jenkins BG, Koroshetz WJ, Beal MF, Rosen BR. Evidence for impairment of energy metabolism in vivo in Huntington's disease using localized 1H NMR spectroscopy. Neurology. 1993;43:2689–95.
   PubMed Web of Science ®Google Scholar
• Jenkins BG, Rosas HD, Chen YC, Makabe T, Myers R, MacDonald M, . 1H NMR spectroscopy studies of Huntington's disease: correlations with CAG repeat numbers. Neurology. 1998;50:1357–65.
   PubMed Web of Science ®Google Scholar
• Basser PJ, Pierpaoli C. Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B. 1996;111:209–19.
   PubMedGoogle Scholar
• Pierpaoli C, Jezzard P, Basser PJ, Barnett A, di Chiro G. Diffusion tensor MR imaging of the human brain. Radiology. 1996;201:637–48.
   PubMed Web of Science ®Google Scholar
• Mori S, Zhang J. Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron. 2006;51:527–39.
   PubMed Web of Science ®Google Scholar
• Basser PJ, Mattiello J, LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophys J. 1994;66:259–67.
   PubMed Web of Science ®Google Scholar
• Turner MR, Grosskreutz J, Kassubek J, Abrahams S, Agosta F, Benatar M, . Towards a neuroimaging biomarker for amyotrophic lateral sclerosis. The Lancet Neurology. 2011 epub;10:400–3.
   PubMed Web of Science ®Google Scholar
• Sun SW, Song SK, Harms MP, Lin SJ, Holtzman DM, Merchant KM, . Detection of age-dependent brain injury in a mouse model of brain amyloidosis associated with Alzheimer's disease using magnetic resonance diffusion tensor imaging. Exp Neurol. 2005;191:77–85.
   PubMed Web of Science ®Google Scholar
• 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 ischaemia. Neuroimage. 2003;20:1714–22.
   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, . Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage. 2005;26:132–40.
   PubMed Web of Science ®Google Scholar
• Filippini N, Douaud G, Mackay CE, Knight S, Talbot K, Turner MR. Corpus callosum involvement is a consistent feature of amyotrophic lateral sclerosis. Neurology. 2010;75:1645–52.
   PubMed Web of Science ®Google Scholar
• Smith MC. Nerve fibre degeneration in the brain in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 1960;23:269–82.
   PubMed Web of Science ®Google Scholar
• Kim JH, Wu TH, Budde MD, Lee JM, Song SK. Non-invasive detection of brainstem and spinal cord axonal degeneration in an amyotrophic lateral sclerosis mouse model. NMR Biomed. 2010;24:163–9.
   PubMedGoogle Scholar
• Underwood CK, Kurniawan ND, Butler TJ, Cowin GJ, Wallace RH. Non-invasive diffusion tensor imaging detects white matter degeneration in the spinal cord of a mouse model of amyotrophic lateral sclerosis. Neuroimage. 2011;55: 455–61.
   PubMedGoogle Scholar
• Engelhardt B. Molecular mechanisms involved in T-cell migration across the blood-brain barrier. J Neural Transm. 2006;113:477–85.
   PubMed Web of Science ®Google Scholar
• Lee SJ, Benveniste EN. Adhesion molecule expression and regulation on cells of the central nervous system. J Neuroimmunol. 1999;98:77–88.
   PubMed Web of Science ®Google Scholar
• Bruck W. The role of macrophages in Wallerian degeneration. Brain Pathol. 1997;7:741–52.
   PubMed Web of Science ®Google Scholar
• Barnett MH, Henderson AP, Prineas JW. The macrophage in MS: just a scavenger after all? Pathology and pathogenesis of the acute MS lesion. Mult Scler. 2006;12:121–32.
   PubMed Web of Science ®Google Scholar
• Turner MR, Cagnin A, Turkheimer FE, Miller CC, Shaw CE, Brooks DJ, . Evidence of widespread cerebral microglial activation in amyotrophic lateral sclerosis: an [(11)C](R)- PK11195 positron emission tomography study. NeurobiolDis. 2004;15:601–9.
   Google Scholar
• Philips T, Robberecht W. Neuroinflammation in amyotrophic lateral sclerosis: role of glial activation in motor neuron disease. Lancet Neurol. 2011 epub;10:253–63.
   PubMed Web of Science ®Google Scholar
• Hall ED, Oostveen JA, Gurney ME. Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia. 1998;23:249–56.
   PubMed Web of Science ®Google Scholar
• Bruijn LI, Becher MW, Lee MK, Anderson KL, Jenkins NA, Copeland NG, . ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron. 1997;18:327–38.
   PubMed Web of Science ®Google Scholar
• Kassa RM, Mariotti R, Bonaconsa M, Bertini G, Bentivoglio M. Gene, cell, and axon changes in the familial amyotrophic lateral sclerosis mouse sensorimotor cortex. J Neuropathol Exp Neurol. 2009;68:59–72.
   PubMed Web of Science ®Google Scholar
• Papadimitriou D, Le Verche V, Jacquier A, Ikiz B, Przedborski S, Re DB. Inflammation in ALS and SMA: sorting out the good from the evil. Neurobiol Dis. 2010;37:493–502.
   PubMed Web of Science ®Google Scholar
• Tada S, Okuno T, Yasui T, Nakatsuji Y, Sugimoto T, Kikutani H, . Deleterious effects of lymphocytes at the early stage of neurodegeneration in an animal model of amyotrophic lateral sclerosis. J Neuroinflammation. 2011;8:19.
   PubMedGoogle Scholar
• Beers DR, Henkel JS, Zhao W, Wang J, Appel SH. CD4 + T-cells support glial neuroprotection, slow disease progression, and modify glial morphology in an animal model of inherited ALS. Proc Natl Acad Sci U S A. 2008;105:15558–63.
   PubMed Web of Science ®Google Scholar
• Banerjee R, Mosley RL, Reynolds AD, Dhar A, Jackson-Lewis V, Gordon PH, . Adaptive immune neuroprotection in G93A-SOD1 amyotrophic lateral sclerosis mice. PLoS One. 2008;3:2740.
   PubMed Web of Science ®Google Scholar
• Chiu IM, Chen A, Zheng Y, Kosaras B, Tsiftsoglou SA, Vartanian TK, . T-lymphocytes potentiate endogenous neuroprotective inflammation in a mouse model of ALS. Proc Natl Acad Sci U S A. 2008;105:17913–8.
   PubMed Web of Science ®Google Scholar
• Garbuzova-Davis S, Haller E, Saporta S, Kolomey I, Nicosia SV, Sanberg PR. Ultrastructure of blood-brain barrier and blood-spinal cord barrier in SOD1 mice modelling ALS. Brain Res. 2007;1157:126–37.
   PubMed Web of Science ®Google Scholar
• Garbuzova-Davis S, Saporta S, Haller E, Kolomey I, Bennett SP, Potter H, . Evidence of compromised blood-spinal cord barrier in early and late symptomatic SOD1 mice modelling ALS. PLoS One. 2007;2:1205.
   PubMed Web of Science ®Google Scholar
• Zhong Z, Deane R, Ali Z, Parisi M, Shapovalov Y, O'Banion MK, . ALS-causing SOD1 mutants generate vascular changes prior to motor neuron degeneration. Nat Neurosci. 2008;11:420–2.
   PubMed Web of Science ®Google Scholar
• Bruck W, Bitsch A, Kolenda H, Bruck Y, Stiefel M, Lassmann H. Inflammatory central nervous system demyelination: correlation of magnetic resonance imaging findings with lesion pathology. Ann Neurol. 1997;42:783–93.
   PubMed Web of Science ®Google Scholar
• Bataveljic D, Stamenkovic S, Bacic G, Andjus PR. Imaging cellular markers of neuroinflammation in the brain of the rat model of amyotrophic lateral sclerosis. Acta Physiol Hung. 2011;98:27–31.
   PubMed Web of Science ®Google Scholar
• Andjus PR, Bataveljic D, Vanhoutte G, Mitrecic D, Pizzolante F, Djogo N, . In vivo morphological changes in animal models of amyotrophic lateral sclerosis and Alzheimer's-like disease: MRI approach. Anat Rec (Hoboken). 2009;292:1882–92.
   PubMedGoogle Scholar
• Verstraete E, Biessels GJ, van den Heuvel MP, Visser F, Luijten PR, van den Berg LH. No evidence of microbleeds in ALS patients at 7 Tesla MRI. Amyotroph Lateral Scler. 2010 epub;11:555–7.
   PubMed Web of Science ®Google Scholar
• Stoll G, Bendszus M. Imaging of inflammation in the peripheral and central nervous system by magnetic resonance imaging. Neuroscience. 2009;158:1151–60.
   PubMedGoogle Scholar
• Zhang Z, van den Bos EJ, Wielopolski PA, der Jong-Popijus M, Bernsen MR, Duncker DJ, . In vitro imaging of single living human umbilical vein endothelial cells with a clinical 3.0-T MRI scanner. MAGMA. 2005;18:175–85.
   PubMedGoogle Scholar
• Mills PH, Ahrens ET. Theoretical MRI contrast model for exogenous T2 agents. Magn Reson Med. 2007;57:442–7.
   PubMedGoogle Scholar
• Cunningham CH, Arai T, Yang PC, McConnell MV, Pauly JM, Conolly SM. Positive contrast magnetic resonance imaging of cells labelled with magnetic nanoparticles. Magn Reson Med. 2005;53:999–1005.
   PubMed Web of Science ®Google Scholar
• Dahnke H, Liu W, Herzka D, Frank JA, Schaeffter T. Susceptibility gradient mapping (SGM): a new post-processing method for positive contrast generation applied to superparamagnetic iron oxide particle (SPIO)-labelled cells. Magn Reson Med. 2008;60:595–603.
   PubMedGoogle Scholar
• Senpan A, Caruthers SD, Rhee I, Mauro NA, Pan D, Hu G, . Conquering the dark side: colloidal iron oxide nanoparticles. ACS Nano. 2009;3:3917–26.
   PubMed Web of Science ®Google Scholar
• Dousset V, Ballarino L, Delalande C, Coussemacq M, Canioni P, Petry KG, . Comparison of ultrasmall particles of iron oxide (USPIO)-enhanced T2-weighted, conventional T2-weighted, and gadolinium-enhanced T1-weighted MR images in rats with experimental autoimmune encephalomyelitis. AJNR Am J Neuroradiol. 1999;20:223–7.
   PubMed Web of Science ®Google Scholar
• Dousset V, Delalande C, Ballarino L, Quesson B, Seilhan D, Coussemacq M, . In vivo macrophage activity imaging in the central nervous system detected by magnetic resonance. Magn Reson Med. 1999;41:329–33.
   PubMed Web of Science ®Google Scholar
• Linker RA, Kroner A, Horn T, Gold R, Maurer M, Bendszus M. Iron particle-enhanced visualization of inflammatory central nervous system lesions by high resolution: preliminary data in an animal model. AJNR Am J Neuroradiol. 2006;27:1225–9.
   PubMedGoogle Scholar
• Rausch M, Hiestand P, Baumann D, Cannet C, Rudin M. MRI-based monitoring of inflammation and tissue damage in acute and chronic relapsing EAE. Magn Reson Med. 2003;50:309–14.
   PubMed Web of Science ®Google Scholar
• Laurent S, Forge D, Port M, Roch A, Robic C, van der Elst L, . Magnetic Iron Oxide Nanoparticles: Synthesis, Stabilization, Vectorization, Physicochemical Characterizations, and Biological Applications. Chem Rev. 2008;108:2064–2110.
   PubMed Web of Science ®Google Scholar
• Bataveljic D, Djogo N, Zupunski L, Bajic A, Nicaise C, Pochet R, . Live monitoring of brain damage in the rat model of amyotrophic lateral sclerosis. Gen Physiol Biophys. 2009;28:212–8.
   PubMedGoogle Scholar
• Machtoub L, Bataveljic D, Andjus PR. Molecular imaging of brain lipid environment of lymphocytes in amyotrophic lateral sclerosis using magnetic resonance imaging and SECARS microscopy. Physiological Research. In press.
   Google Scholar
• Bulte JW, Verkuyl JM, Herynek V, Katsanis E, Brocke S, Holla M, . Magnetoimmunodetection of (transfected) ICAM-1 gene expression. Proceedings of the International Society of Magnetic Resonance Medicine. 1998;6:307.
   Google Scholar
• Schneider C, Schuetz G, Zollner TM. Acute neuroinflammation in Lewis rats: a model for acute multiple sclerosis relapses. J Neuroimmunol. 2009;213:84–90.
   PubMed Web of Science ®Google Scholar
• McAteer MA, Sibson NR, von Zur Muhlen C, Schneider JE, Lowe AS, Warrick N, . In vivo magnetic resonance imaging of acute brain inflammation using microparticles of iron oxide. Nat Med. 2007;13:1253–8.
   PubMed Web of Science ®Google Scholar
• von Zur Muhlen C, von Elverfeldt D, Choudhury RP, Ender J, Ahrens I, Schwarz M, . Functionalized magnetic resonance contrast agent selectively binds to glycoprotein IIb/IIIa on activated human platelets under flow conditions and is detectable at clinically relevant field strengths. Mol Imaging. 2008;7:59–67.
   PubMedGoogle Scholar
• Dupuis L, Spreux-Varoquaux O, Bensimon G, Jullien P, Lacomblez L, Salachas F, . Platelet serotonin level predicts survival in amyotrophic lateral sclerosis. PLoS One. 2010 epub;5:13346.
   PubMed Web of Science ®Google Scholar
• Shrivastava M, Das TK, Behari M, Pati U, Vivekanandhan S. Ultrastructural variations in platelets and platelet mitochondria: a novel feature in amyotrophic lateral sclerosis. Ultrastruct Pathol. 2011;35:52–9.
   PubMed Web of Science ®Google Scholar
• Serres S, Anthony DC, Jiang Y, Broom KA, Campbell SJ, Tyler DJ, . Systemic inflammatory response reactivates immune-mediated lesions in rat brain. J Neurosci. 2009;29:4820–8.
   PubMed Web of Science ®Google Scholar
• van Kasteren SI, Campbell SJ, Serres S, Anthony DC, Sibson NR, Davis BG. Glyconanoparticles allow pre-symptomatic in vivo imaging of brain disease. Proc Natl Acad Sci U S A. 2009;106:18–23.
   PubMedGoogle Scholar
• Vernon AC, Ballard C, Modo M. Neuroimaging for Lewy body disease: is the in vivo molecular imaging of alpha-synuclein neuropathology required and feasible? Brain Res Rev. 2010;65:28–55.
   PubMedGoogle Scholar
• Aoki I, Tanaka C, Takegami T, Ebisu T, Umeda M, Fukunaga M, . Dynamic activity-induced manganese-dependent contrast magnetic resonance imaging (DAIM MRI). Magn Reson Med. 2002;48:927–33.
   PubMed Web of Science ®Google Scholar
• Duong TQ, Silva AC, Lee SP, Kim SG. Functional MRI of calcium-dependent synaptic activity: cross-correlation with CBF and BOLD measurements. Magn Reson Med. 2000;43:383–92.
   PubMed Web of Science ®Google Scholar
• Brurok H, Skoglund T, Berg K, Skarra S, Karlsson JO, Jynge P. Myocardial manganese elevation and proton relaxivity enhancement with manganese dipyridoxyl diphosphate. Ex vivo assessments in normally perfused and ischaemic guinea pig hearts. NMR Biomed. 1999;12:364–72.
   PubMed Web of Science ®Google Scholar
• Saleem KS, Pauls JM, Augath M, Trinath T, Prause BA, Hashikawa T, . Magnetic resonance imaging of neuronal connections in the Macaque monkey. Neuron. 2002;34:685–700.
   PubMedGoogle Scholar
• van der Linden A, Verhoye M, van Meir V, Tindemans I, Eens M, Absil P, . In vivo manganese-enhanced magnetic resonance imaging reveals connections and functional properties of the songbird vocal control system. Neuroscience. 2002;112:467–74.
   PubMedGoogle Scholar
• Aoki I, Wu YJ, Silva AC, Lynch RM, Koretsky AP. In vivo detection of neuroarchitecture in the rodent brain using manganese-enhanced MRI. Neuroimage. 2004;22:1046–59.
   PubMed Web of Science ®Google Scholar
• Silva AC, Bock NA. Manganese-enhanced MRI: an exceptional tool in translational neuroimaging. Schizophr Bull. 2008;34:595–604.
   PubMed Web of Science ®Google Scholar
• Bilgen M, Al-Hafez B, Berman NE, Festoff BW. Magnetic resonance imaging of mouse spinal cord. Magn Reson Med. 2005;54:1226–31.
   PubMed Web of Science ®Google Scholar
• Ravits JM, La Spada AR. ALS motor phenotype heterogeneity, focality, and spread: deconstructing motor neuron degeneration. Neurology. 2009;73:805–11.
   PubMed Web of Science ®Google Scholar
• Mohammadi B, Kollewe K, Samii A, Krampfl K, Dengler R, Munte TF. Changes of resting state brain networks in amyotrophic lateral sclerosis. Exp Neurol. 2009;217:147–53.
   PubMed Web of Science ®Google Scholar
• Jelsone-Swain LM, Fling BW, Seidler RD, Hovatter R, Gruis K, Welsh RC. Reduced interhemispheric functional connectivity in the motor cortex during rest in limb-onset amyotrophic lateral sclerosis. Frontiers in Systems Neuroscience. (Original Research). 2010;1:12.
   Google Scholar
• Martin C, Sibson NR. Pharmacological MRI in animal models: a useful tool for 5-HT research? Neuropharmacology. 2008;55:1038–47.
   PubMedGoogle Scholar
• Rule RR, Schuff N, Miller RG, Weiner MW. Gray matter perfusion correlates with disease severity in ALS. Neurology. 2010;74:821–7.
   PubMed Web of Science ®Google Scholar
• Choi JK, Dedeoglu A, Jenkins BG. Longitudinal monitoring of motor neuron circuitry in FALS rats using in vivo phMRI. Neuroreport. 2010;21:157–62.
   PubMedGoogle Scholar
• Hajnal JV, Myers R, Oatridge A, Schwiesto JE, Young IR, Bydder GM. Artifacts due to stimulus correlated motion in functional imaging of the brain. Magn Reson Med. 1994;31:283–91.
   PubMedGoogle Scholar
• Austin VC, Blamire AM, Allers KA, Sharp T, Styles P, Matthews PM, . Confounding effects of anaesthesia on functional activation in rodent brain: a study of halothane and alpha-chloralose anaesthesia. Neuroimage. 2005; 24:92–100.
   PubMedGoogle Scholar
• Martin C, Martindale J, Berwick J, Mayhew J. Investigating neural-haemodynamic coupling and the haemodynamic response function in the awake rat. Neuroimage. 2006;32:33–48.
   PubMedGoogle Scholar
• Febo M, Segarra AC, Nair G, Schmidt K, Duong TQ, Ferris CF. The neural consequences of repeated cocaine exposure revealed by functional MRI in awake rats. Neuro-psychopharmacology. 2005;30:936–43.
   Google Scholar
• King JA, Garelick TS, Brevard ME, Chen W, Messenger TL, Duong TQ, . Procedure for minimizing stress for fMRI studies in conscious rats. J Neurosci Methods. 2005;148: 154–60.
   PubMed Web of Science ®Google Scholar
• Tabuchi E, Yokawa T, Mallick H, Inubushi T, Kondoh T, Ono T, . Spatio-temporal dynamics of brain activated regions during drinking behaviour in rats. Brain Res. 2002;951:270–9.
   PubMed Web of Science ®Google Scholar
• Wong PC, Pardo CA, Borchelt DR, Lee MK, Copeland NG, Jenkins NA, . An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron. 1995;14:1105–16.
   PubMed Web of Science ®Google Scholar
• Schmitt-John T, Drepper C, Mussmann A, Hahn P, Kuhlmann M, Thiel C, . Mutation of Vps54 causes motor neuron disease and defective spermiogenesis in the Wobbler mouse. Nat Genet. 2005;37:1213–5.
   PubMed Web of Science ®Google Scholar
• Nagai M, Aoki M, Miyoshi I, Kato M, Pasinelli P, Kasai N, . Rats expressing human cytosolic copper-zinc superoxide dismutase transgenes with amyotrophic lateral sclerosis: associated mutations develop motor neuron disease. J Neurosci. 2001;21:9246–54.
   PubMed Web of Science ®Google Scholar
• Hafezparast M, Klocke R, Ruhrberg C, Marquardt A, Ahmad-Annuar A, Bowen S, . Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science. 2003;300:808–12.
   PubMed Web of Science ®Google Scholar
• Wegorzewska I, Bell S, Cairns NJ, Miller TM, Baloh RH. TDP-43 mutant transgenic mice develop features of ALS and frontotemporal lobar degeneration. Proc Natl Acad Sci U S A. 2009;106:18809–14.
   PubMed Web of Science ®Google Scholar
• Huang C, Zhou H, Tong J, Chen H, Liu YJ, Wang D, . FUS Transgenic Rats Develop the Phenotypes of Amyotrophic Lateral Sclerosis and Frontotemporal Lobar Degeneration. PLoS Genet. 2011;7:1002011.
   PubMed Web of Science ®Google Scholar
• Tudor EL, Galtrey CM, Perkinton MS, Lau KF, de Vos KJ, Mitchell JC, . Amyotrophic lateral sclerosis mutant vesicle-associated membrane protein-associated protein-B transgenic mice develop TAR-DNA-binding protein-43 pathology. Neuroscience. 2010;167:774–85.
   PubMed Web of Science ®Google Scholar
• Birken DL, Oldendorf WH. N-acetyl-L-aspartic acid: a literature review of a compound prominent in 1H-NMR spectroscopic studies of brain. Neurosci Biobehav Rev. 1989;13:23–31.
   PubMed Web of Science ®Google Scholar
• Kantarci K, Reynolds G, Petersen RC, Boeve BF, Knopman DS, Edland SD, . Proton MR spectroscopy in mild cognitive impairment and Alzheimer's disease: comparison of 1.5 and 3 T. AJNR Am J Neuroradiol. 2003;24:843–9.
   PubMed Web of Science ®Google Scholar
• Smith JK, Castillo M, Kwock L. MR spectroscopy of brain tumours. Magn Reson Imaging Clin N Am. 2003;11:415–29.
   PubMedGoogle Scholar
• Bottomley PA, Lee Y, Weiss RG. Total creatine in muscle: imaging and quantification with proton MR spectroscopy. Radiology. 1997;204:403–10.
   PubMed Web of Science ®Google Scholar
• Magistretti PJ, Pellerin L, Rothman DL, Shulman RG. Energy on demand. Science. 1999;283:496–7.
   PubMed Web of Science ®Google Scholar
• Jenkins BG, Klivenyi P, Kustermann E, Andreassen OA, Ferrante RJ, Rosen BR, . Non-linear decrease over time in N-acetyl aspartate levels in the absence of neuronal loss and increases in glutamine and glucose in transgenic Huntington's disease mice. J Neurochem. 2000;74:2108–19.
   PubMed Web of Science ®Google Scholar
• Brand A, Richter-Landsberg C, Leibfritz D. Multinuclear NMR studies on the energy metabolism of glial and neuronal cells. Dev Neurosci. 1993;15:289–98.
   PubMed Web of Science ®Google Scholar
• Thurston JH, Sherman WR, Hauhart RE, Kloepper RF. Myo-inositol: a newly identified non-nitrogenous osmoregulatory molecule in mammalian brain. Pediatr Res. 1989;26:482–5.
   PubMed Web of Science ®Google Scholar
• Alexianu ME, Kozovska M, Appel SH. Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology. 2001;57:1282–9.
   PubMed Web of Science ®Google Scholar
• Hoyte LC, Brooks KJ, Nagel S, Akhtar A, Chen R, Mardiguian S, . Molecular magnetic resonance imaging of acute vascular cell adhesion molecule-1 expression in a mouse model of cerebral ischaemia. J Cereb Blood Flow Metab. 2010 epub;30:1178–87.
   PubMedGoogle Scholar
• McAteer MA, Schneider JE, Ali ZA, Warrick N, Bursill CA, von zur Muhlen C, . Magnetic resonance imaging of endothelial adhesion molecules in mouse atherosclerosis using dual-targeted microparticles of iron oxide. Arterioscler Thromb Vasc Biol. 2008;28:77–83.
   PubMed Web of Science ®Google Scholar
• Gowing G, Philips T, van Wijmeersch B, Audet JN, Dewil M, van den Bosch L, . Ablation of proliferating microglia does not affect motor neuron degeneration in amyotrophic lateral sclerosis caused by mutant superoxide dismutase. J Neurosci. 2008;28:10234–44.
   PubMed Web of Science ®Google Scholar
• Guilfoyle DN, Helpern JA, Lim KO. Diffusion tensor imaging in fixed brain tissue at 7.0 T. NMR Biomed. 2003;16:77–81.
   PubMedGoogle Scholar