Abstract
Amyotrophic lateral sclerosis (ALS) is a fatal progressive disorder of the central nervous system affecting the upper and lower motor neurons. It is important to study the specific nature of the disease course and the character of neurodegenerative process expansion in ALS, since no effective methods of treatment for this disease have been developed yet. Despite the clear evidence of multisystem brain damage in ALS, there are no objective biomarkers of the upper motor neuron lesion and extramotor brain areas involvement. In recent years, structural and functional neuroimaging, such as MR-morphometry, diffusion-tensor magnetic resonance imaging, MR spectroscopy, functional MRI, positron emission tomography (PET), etc., have been playing a significant role in research on ALS. This review analyzes the results of neuroimaging methods in the context of their application for diagnostics, prediction, and monitoring the ALS course. The most sensitive and specific techniques to diagnose the disease are diffusion-tensor MRI, MR spectroscopy, PET, a combination of several neuroimaging methods, and neuroimaging with transcranial magnetic stimulation. Diffusion-tensor MRI and MR spectroscopy can be used to monitor and predict the disease course. The main limitations and weak points of the published studies on this topic, as well as the prospective for neuroimaging in ALS, are discussed.
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REFERENCES
Bokovoi amiotroficheskii skleroz (Amyotrophic Lateral Sclerosis), Zavalishin, I.A., Ed., Moscow: Evraziya+, 2007.
Zakharova, M.N., Illarioshkin, S.N., Abramyche-va, N.Yu., et al., Amyotrophic lateral sclerosis, in Nevrologiya. Natsional’noe rukovodstvo (Neurology: National Guide), Gusev, E.I., Konovalov, A.N., and Gekht, A.B., Eds., Moscow: GEOTAR-Media, 2014, pp. 420–439.
Turner, M.R. and Swash, M., The expanding syndrome of amyotrophic lateral sclerosis: a clinical and molecular odyssey, J. Neurol. Neurosurg. Psychiatry, 2015, vol. 86, no. 6, pp. 667–673. PMID 25644224. doi 10.1136/jnnp-2014-308946
Phukan, J., Elamin, M., Bede, P., et al., The syndrome of cognitive impairment in amyotrophic lateral sclerosis: a population-based study, J. Neurol. Neurosurg. Psychiatry, 2012, vol. 83, pp. 102–108. PMID 21836033. doi 10.1136/jnnp-2011-300188
Blasco, H., Vourc’h, P., Pradat, P.F., et al., Further development of biomarkers in amyotrophic lateral sclerosis, Exp. Rev. Mol. Diagn., 2016, vol. 16, no. 8, pp. 853–868. PMID 27275785. doi 10.1080/ 14737159.2016.1199277
Kraemer, M., Buerger, M., and Berlit, P., Diagnostic problems and delay of diagnosis in amyotrophic lateral sclerosis, Clin. Neurol. Neurosurg., 2010, vol. 112, no. 2, pp. 103–105. PMID 27275785. doi 10.1080/ 14737159.2016.1199277
Illarioshkin, S.N., Tanashyan, M.M., Maksimo-va, M.Yu., et al., The concept of biomarkers in clinical neurology: the possibility of early diagnosis and prognosis of individual risk, in Nevrologiya XXI veka: diagnosticheskie, lechebnye i issledovatel’skie tekhnologii. Rukovodstvo dlya vrachei (Neurology of 21 Century: Diagnostics, Medical Course, and Study Technologies. Manual for Physicians), Piradov, M.A., Illarioshkin, S.N., and Tanashyan, M.M., Eds., Moscow: ATMO, 2015, vol. 3, pp. 363–424.
Turner, M.R. and Verstraete, E., What does imaging reveal about the pathology of amyotrophic lateral sclerosis? Curr. Neurol. Neurosci. Rep., 2015, vol. 15, no. 7, p. 45. PMID 26008817. doi 10.1007/s11910-015-0569-6
Chiò, A., Pagani, M., Agosta, F., et al., Neuroimaging in amyotrophic lateral sclerosis: insights into structural and functional changes, Lancet Neurol., 2014, vol. 13, no. 12, pp. 1228–1240. PMID 25453462. doi 10.1016/S1474-4422(14)70167-X
Pradat, P.F. and El Mendili, M.M., Neuroimaging to investigate multisystem involvement and provide biomarkers in amyotrophic lateral sclerosis, Biomed. Res. Int., 2014, vol. 2014, p. 467560. PMID 24949452. doi 10.1155/2014/467560
Piradov, M.A., Tanashyan, M.M., Krotenkova, M.V., et al., State-of-the-art neuroimaging techniques, Ann. Klin. Eksp. Nevrol., 2015, vol. 9, no. 4, pp. 13–20.
Kremneva, E.I., Vorob’eva, A.A., and Adarcheva, L.S., Forewarned is forearmed: MRI practical aspects in Hirayama disease, Luchevaya Diagn. Ter., 2015, vol. 6, no. 3, pp. 35–43.
Bede, P. and Hardiman, O., Lessons of ALS imaging: Pitfalls and future directions—a critical review, Neuroimage Clin., 2014, vol. 4, pp. 436–443. PMID 24624329. doi 10.1016/j.nicl.2014.02.011
Foerster, B.R., Welsh, R.C., and Feldman, E.L., 25 years of neuroimaging in amyotrophic lateral sclerosis, Nat. Rev. Neurol., 2013, vol. 9, no. 9, pp. 513–524. PMID 23917850. doi 10.1038/nrneurol.2013.153
Sabatelli, M., Conte, A., and Zollino, M., Clinical and genetic heterogeneity of amyotrophic lateral sclerosis, Clin. Genet., 2013, vol. 83, no. 5, pp. 408–16. PMID 23379621. doi 10.1111/cge.12117
Leblond, C.S., Kaneb, H.M., Dion, P.A., and Rouleau, G.A., Dissection of genetic factors associated with amyotrophic lateral sclerosis, Exp. Neurol., 2014, vol. 262, pp. 91–101. PMID 24780888. doi 10.1016/ j.expneurol.2014.04.013
Swinnen, B. and Robberecht, W., The phenotypic variability of amyotrophic lateral sclerosis, Nat. Rev. Neurol., 2014, vol. 10, pp. 661–670. PMID 25311585. doi 10.1038/nrneurol.2014.184
Jawdat, O., Statland, J.M., and Barohn, R.J., Amyotrophic lateral sclerosis regional variants (brachial amyotrophic diplegia, leg amyotrophic diplegia, and isolated bulbar amyotrophic lateral sclerosis), Neurol. Clin., 2015, vol. 33, no. 4, pp. 775–785. PMID 26515621. doi 10.1016/j.ncl.2015.07.003
Beghi, E., Chiò, A., Couratier, P. et al., The epidemiology and treatment of ALS: focus on the heterogeneity of the disease and critical appraisal of therapeutic trials, Amyotrophic Lateral Scler. Other Mot. Neuron Disord., 2011, vol. 12, pp. 1–10. PMID 20698807. doi 10.3109/ 17482968.2010.502940
Traynor, B.J., Codd, M.B., Corr, B., et al., Clinical features of amyotrophic lateral sclerosis according to the El Escorial and Airlie House diagnostic criteria: A population-based study, Arch. Neurol., 2000, vol. 57, no. 8, pp. 1171–1176. PMID 10927797
Swash, M., Why are upper motor neuron signs difficult to elicit in amyotrophic lateral sclerosis? J. Neurol. Neurosurg. Psychiatry, 2012, vol. 83, no. 6, pp. 659–662. PMID 22496581. doi 10.1136/jnnp-2012-302315
Bakulin, I.S., Chervyakov, A.V., and Zakharova, M.N., Navigated transcranial magnetic stimulation possibilities in difficult diagnostic cases upper motor neuron lesions—case report, Nervno-Myshechnye Bolezni, 2015, no. 2, pp. 32–37.
Huynh, W., Simon, N.G., Grosskreutz, J., et al., Assessment of the upper motor neuron in amyotrophic lateral sclerosis, Clin. Neurophysiol., 2016, vol. 127, no. 7, pp. 2643–2660. PMID 27291884. doi 10.1016/ j.clinph.2016.04.025
Verstraete, E. and Foerster, B.R., Neuroimaging as a new diagnostic modality in amyotrophic lateral sclerosis, Neurotherapeutics, 2015, vol. 12, no. 2, pp. 403–416. PMID 25791072. doi 10.1007/s13311-015-0347-9
Stuchevskaya, T.R., Tyutin, L.A., Pozdnyakov, A.V., et al., Brain magnetic resonance imaging in patients with classical amyotrophic lateral sclerosis and its atypical variants, Nevrol. Zh., 2015, vol. 20, no. 4, pp. 29–35.
Huynh, W., Lam, A., Vucic, S., et al., Corticospinal tract dysfunction and development of amyotrophic lateral sclerosis following electrical injury, Muscle Nerve, 2010, vol. 42, pp. 288–292. PMID 20589889. doi 10.1002/mus.21681
da Rocha, A.J. and Maia Júnior, A.C.M., Is magnetic resonance imaging a plausible biomarker for upper motor neuron degeneration in amyotrophic lateral sclerosis/primary lateral sclerosis or merely a useful paraclinical tool to exclude mimic syndromes? A critical review of imaging applicability in clinical routine, Arq. Neuro-Psiquiatr., 2012, vol. 70, pp. 532–539. PMID 22836461
Hecht, M.J., Fellner, F., and Fellner, C., Hyperintense and hypointense MRI signals of the precentral gyrus and corticospinal tract in ALS: a follow-up examination including FLAIR images, J. Neurol. Sci., 2002, vol. 199, nos. 1–2, pp. 59–65. PMID 12084444
Jin, J., Hu, F., Zhang, Q., et al., Hyperintensity of the corticospinal tract on FLAIR: A simple and sensitive objective upper motor neuron degeneration marker in clinically verified amyotrophic lateral sclerosis, J. Neurol. Sci., 2016, vol. 367, pp. 177–183. PMID 27423585. doi 10.1016/j.jns.2016.06.005
Pronin, I.N., Fadeeva, L.M., Zakharova, N.E., et al., Diffusion tensor imaging and diffusion tensor tractography, Ann. Klin. Eksp. Nevrol., 2008, vol. 2, no. 1, pp. 32–41.
Foerster, B.R., Dwamena, B.A., Petrou, M., et al., Diagnostic accuracy of diffusion tensor imaging in amyotrophic lateral sclerosis: a systematic review and individual patient data meta-analysis, Acad. Radiol., 2013, vol. 20, no. 9, pp. 1099–1106. PMID 23931423. doi 10.1016/j.acra.2013.03.017
Ben Bashat, D., Artzi, M., Tarrasch, R., et al., A potential tool for the diagnosis of ALS based on diffusion tensor imaging, Amyotrophic Lateral Scler., 2011, vol. 12, no. 6, pp. 398–405. doi 10.3109/17482968.2011.582646
Schuster, C., Elamin, M., Hardiman, O., and Bede, P., The segmental diffusivity profile of amyotrophic lateral sclerosis associated white matter degeneration, Eur. J. Neurol., 2016, vol. 23, no. 8, pp. 1361–1371. doi 10.1111/ene.13038
Filippini, N., Douaud, G., Mackay, C.E., et al., Corpus callosum involvement is a consistent feature of amyotrophic lateral sclerosis, Neurology, 2010, vol. 75, no. 18, pp. 1645–1652. PMID 21041787. doi 10.1212/WNL.0b013e3181fb84d1
Kaufmann, P., Pullman, S.L., Shungu, D.C., et al., Objective tests for upper motor neuron involvement in amyotrophic lateral sclerosis (ALS), Neurology, 2004, vol. 62, pp. 1753–1757. PMID 15159473
Kalra, S., Hanstock, C.C., Martin, W.R., et al., Detection of cerebral degeneration in amyotrophic lateral sclerosis using high-field magnetic resonance spectroscopy, Arch. Neurol., 2006, vol. 63, pp. 1144–1148. PMID 16908742. doi 10.1001/archneur.63.8.1144
Zhu, H., Edden, R.A., Ouwerkerk, R., et al., High resolution spectroscopic imaging of GABA at 3 Tesla, Magn. Reson. Med., 2011, vol. 65, no. 3, pp. 603–609. PMID 21337399. doi 10.1002/mrm.22671
Foerster, B.R., Callaghan, B.C., Petrou, M., et al., Decreased motor cortex gamma-aminobutyric acid in amyotrophic lateral sclerosis, Neurology, 2012, vol. 78, no. 20, pp. 1596–1600. PMID 22517106. doi 10.1212/ WNL.0b013e3182563b57
Verstraete, E., Veldink, J.H., Hendrikse, J., et al., Structural MRI reveals cortical thinning in amyotrophic lateral sclerosis, J. Neurol. Neurosurg. Psychiatry, 2012, vol. 83, pp. 383–388. PMID 21965521. doi 10.1136/jnnp-2011-300909
Walhout, R., Westeneng, H.J., Verstraete, E., et al., Cortical thickness in ALS: towards a marker for upper motor neuron involvement, J. Neurol. Neurosurg. Psychiatry, 2015, vol. 86, pp. 288–294. PMID 25121571. doi 10.1136/jnnp-2013-306839
Agosta, F., Valsasina, P., Riva, N., et al., The cortical signature of amyotrophic lateral sclerosis, PLoS One, 2012, vol. 7, no. 8, p. 42816. PMID 22880116. doi 10.1371/journal.pone.0042816
Chen, Z. and Ma, L., Grey matter volume changes over the whole brain in amyotrophic lateral sclerosis: a voxel-wise meta-analysis of voxel based morphometry studies, Amyotrophic Lateral Scler., 2010, vol. 11, pp. 549–554. PMID 20929296. doi 10.3109/ 17482968.2010.516265
Dalakas, M.C., Hatazawa, J., Brooks, R.A., and Di Chiro, G., Lowered cerebral glucose utilization in amyotrophic lateral sclerosis, Ann. Neurol., 1987, vol. 22, pp. 580–586. PMID 3501273. doi 10.1002/ana. 410220504
Hoffman, J.M., Mazziotta, J.C., Hawk, T.C., and Sumida, R., Cerebral glucose utilization in motor neuron disease, Arch. Neurol., 1992, vol. 49, pp. 849–854. PMID 1524517
Pagani, M., Chiò, A., Valentini, M.C., et al., FDG-PET in amyotrophic lateral sclerosis—functional pattern and diagnostic accuracy, Neurology, 2014, vol. 83, pp. 1067–1074. PMID 26940764. doi 10.2967/ jnumed.115.166272
van Laere, K., Vanhee, A., Verschueren, J., et al., Value of 18fluorodeoxyglucose-positron-emission tomography in amyotrophic lateral sclerosis: a prospective study, J.A.M.A. Neurol., 2014, vol. 71, pp. 553–561. PMID 24615479. doi 10.1001/ jamaneurol.2014.62
Foerster, B.R., Carlos, R.C., Dwamena, B.A., et al., Multimodal MRI as a diagnostic biomarker for amyotrophic lateral sclerosis, Ann. Clin. Transl. Neurol., 2014, vol. 1, pp. 107–114. PMID 25356389. doi 10.1002/acn3.30
Cervo, A., Cocozza, S., Sacca, F., et al., The combined use of conventional MRI and MR spectroscopic imaging increases the diagnostic accuracy in amyotrophic lateral sclerosis, Eur. J. Radiol., 2015, vol. 84, pp. 151–157. PMID 25466774. doi 10.1016/j.ejrad.2014.10.019
Pohl, C., Block, W., Traber, F., et al., Proton magnetic resonance spectroscopy and transcranial magnetic stimulation for the detection of upper motor neuron degeneration in ALS patients, J. Neurol. Sci., 2001, vol. 190, pp. 21–27. PMID 11574102
Furtula, J., Johnsen, B., Frandsen, J., et al., Upper motor neuron involvement in amyotrophic lateral sclerosis evaluated by triple stimulation technique and diffusion tensor MRI, J. Neurol., 2013, vol. 260, no. 6, pp. 1535–1544. PMID 23299622. doi 10.1007/s00415-012-6824-8
Bae, J.S., Ferguson, M., Tan, R., et al., Dissociation of structural and functional integrities of the motor system in amyotrophic lateral sclerosis and behavioral-variant frontotemporal dementia, J. Clin. Neurol., 2016, vol. 12, no. 2, pp. 209–217. PMID 26932257. doi 10.3988/jcn.2016.12.2.209
Qureshi, M., Schoenfeld, D.A., Paliwal, Y., et al., The natural history of ALS is changing: improved survival, Amyotrophic Lateral Scler. Other Mot. Neuron Disord., 2009, vol. 10, pp. 324–331. PMID 19922119. doi 10.3109/17482960903009054
Rutkove, S.B., Clinical measures of disease progression in amyotrophic lateral sclerosis, Neurotherapeutics, 2015, vol. 12, no. 2, pp. 384–393. PMID 25582382. doi 10.1007/s13311-014-0331-9
Mitsumoto, H., Brooks, B.R., and Silani, V., Clinical trials in amyotrophic lateral sclerosis: why so many negative trials and how can trials be improved? Lancet Neurol., 2014, vol. 13, no. 11, pp. 1127–1138. PMID 25316019. doi 10.1016/S1474-4422(14)70129-2
Keil, C., Prell, T., Peschel, T., et al., Longitudinal diffusion tensor imaging in amyotrophic lateral sclerosis, BMC Neurosci., 2012, vol. 13, p. 141. PMID 23134591. doi 10.1186/1471-2202-13-141
Menke, R.A., Abraham, I., Thiel, C.S., et al., Fractional anisotropy in the posterior limb of the internal capsule and prognosis in amyotrophic lateral sclerosis, Arch. Neurol., 2012, vol. 69, pp. 1493–1499. PMID 22910997. doi 10.1001/archneurol.2012.1122
van der Graaff, M.M., Sage, C.A., Caan, M.W., et al., Upper and extramotoneuron involvement in early motoneuron disease: a diffusion tensor imaging study, Brain, 2011, vol. 134, pp. 1211–1228. PMID 21362631. doi 10.1093/brain/awr016
Sage, C.A., Peeters, R.R., Gorner, A., et al., Quantitative diffusion tensor imaging in amyotrophic lateral sclerosis, NeuroImage, 2007, vol. 34, pp. 486–499. PMID 17097892. doi 10.1016/j.neuroimage. 2006.09.025
Kwan, J.Y., Meoded, A., Danielian, L.E., et al., Structural imaging differences and longitudinal changes in primary lateral sclerosis and amyotrophic lateral sclerosis, Neuroimage Clin., 2013, vol. 2, pp. 151–160. PMID 24179768. doi 10.1016/j.nicl.2012.12.003
Agosta, F., Rocca, M.A., Valsasina, P., et al., A longitudinal diffusion tensor MRI study of the cervical cord and brain in amyotrophic lateral sclerosis patients, J. Neurol. Neurosurg. Psychiatry, 2009, vol. 80, no. 1, pp. 53–55. PMID 18931009. doi 10.1136/ jnnp.2008.154252
Blain, C.R., Williams, V.C., Johnston, C., et al., A longitudinal study of diffusion tensor MRI in ALS, Amyotrophic Lateral Scler., 2007, vol. 8, no. 6, pp. 348–355. PMID 17924235. doi 10.1080/17482960701548139
Mitsumoto, H., Ulug, A.M., Pullman, S.L., et al., Quantitative objective markers for upper and lower motor neuron dysfunction in ALS, Neurology, 2007, vol. 68, no. 17, pp. 1402–1410. PMID 17452585. doi 10.1212/01.wnl.0000260065.57832.87
Senda, J., Kato, S., Kaga, T., et al., Progressive and widespread brain damage in ALS: MRI voxel-based morphometry and diffusion tensor imaging study, Amyotrophic Lateral Scler., 2011, vol. 12, no. 1, pp. 59–69. PMID 21271792. doi 10.3109/17482968.2010.517850
Zhang, Y., Schuff, N., Woolley, S.C., et al., Progression of white matter degeneration in amyotrophic lateral sclerosis: a diffusion tensor imaging study, Amyotrophic Lateral Scler., 2011, vol. 12, no. 6, pp. 421–429. PMID 21745124. doi 10.3109/17482968.2011.593036
Agosta, F., Gorno-Tempini, M.L., Pagani, E., et al., Longitudinal assessment of grey matter contraction in amyotrophic lateral sclerosis: a tensor based morphometry study, Amyotrophic Lateral Scler., 2009, vol. 10, no. 3, pp. 168–74. PMID 19058055. doi 10.1080/ 17482960802603841
Cardenas-Blanco, A., Machts, J., Acosta-Cabronero, J., et al., Structural and diffusion imaging versus clinical assessment to monitor amyotrophic lateral sclerosis, Neuroimage Clin., 2016, vol. 11, pp. 408–414. PMID 27104135. doi 10.1016/j.nicl.2016.03.011.
Block, W., Karitzky, J., Traber, F., et al., Proton magnetic resonance spectroscopy of the primary motor cortex in patients with motor neuron disease: sub group analysis and follow-up measurements, Arch. Neurol., 1998, vol. 55, no. 7, pp. 931–936. PMID 9678310
Pohl, C., Block, W., Karitzky, J., et al., Proton magnetic resonance spectroscopy of the motor cortex in 70 patients with amyotrophic lateral sclerosis, Arch. Neurol., 2001, vol. 58, no. 5, pp. 729–735. PMID 11346367
Block, W., Traber, F., Flacke, S., et al., In-vivo proton MR-spectroscopy of the human brain: assessment of N-acetylaspartate (NAA) reduction as a marker for neurodegeneration, Amino Acids, 2002, vol. 23, nos. 1–3, pp. 317–323. PMID 12373553. doi 10.1007/s00726-001-0144-0
Suhy, J., Miller, R.G., Rule, R., et al., Early detection and longitudinal changes in amyotrophic lateral sclerosis by 1H MRSI, Neurology, 2002, vol. 58, no. 5, pp. 773–779. PMID 11889242
Rule, R.R., Suhy, J., Schuff, N., et al., Reduced NAA in motor and non-motor brain regions in amyotrophic lateral sclerosis: a cross-sectional and longitudinal study, Amyotrophic Lateral Scler. Other Mot. Neuron Disord., 2004, vol. 5, no. 3, pp. 141–149. PMID 15512902. doi 10.1080/14660820410017109
Unrath, A., Ludolph, A.C., and Kassubek, J., Brain metabolites in definite amyotrophic lateral sclerosis. A longitudinal proton magnetic resonance spectroscopy study, J. Neurol., 2007, vol. 254, no. 8, pp. 1099–1106. PMID 17431700. doi 10.1007/s00415-006-0495-2
Kalra, S., Tai, P., Genge, A., and Arnold, D.L., Rapid improvement in cortical neuronal integrity in amyotrophic lateral sclerosis detected by proton magnetic resonance spectroscopic imaging, J. Neurol., 2006, vol. 253, no. 8, pp. 1060–1063. PMID 16609809. doi 10.1007/s00415-006-0162-7
Lee, S. and Kim, H.J., Prion-like mechanism in amyotrophic lateral sclerosis: are protein aggregates the key? Exp. Neurobiol., 2015, vol. 24, no. 1, pp. 1–7. PMID 25792864. doi 10.5607/en.2015.24.1.1.
Grad, L.I., Fernando, S.M., and Cashman, N.R., From molecule to molecule and cell to cell: prion-like mechanisms in amyotrophic lateral sclerosis, Neurobiol. Dis., 2015, vol. 77, pp. 257–265. PMID 25701498. doi 10.1016/j.nbd.2015.02.009
Schmidt, R., Verstraete, E., de Reus, M.A., et al., Correlation between structural and functional connectivity impairment in amyotrophic lateral sclerosis, Hum. Brain Mapp., 2014, vol. 35, no. 9, pp. 4386–4395. PMID 24604691. doi 10.1002/hbm.22481
Lysogorskaya, E.V., Abramycheva, N.Y., Illarioshkin, S.N., and Zakharova, M.N., The role of RNA metabolism in the pathogenesis of amyotrophic lateral sclerosis, Neirokhim. Zh., 2012, no. 3, pp. 247–252.
Brettschneider, J., Del Tredici, K., Toledo, J.B., et al., Stages of pTDP-43 pathology in amyotrophic lateral sclerosis, Ann. Neurol., 2013, vol. 74, no. 1, pp. 20–38. PMID 23686809. doi 10.1002/ana.23937
Kassubek, J., Muller, H.P., Del Tredici, K., et al., Diffusion tensor imaging analysis of sequential spreading of disease in amyotrophic lateral sclerosis confirms patterns of TDP-43 pathology, Brain, 2014, vol. 137, no. 6, pp. 1733–1740. PMID 24736303. doi 10.1093/ brain/awu090
Pupillo, E., Messina, P., Logroscino, G., et al., Long-term survival in amyotrophic lateral sclerosis: a population-based study, Ann. Neurol., 2014, vol. 75, no. 2, pp. 287–297. PMID 24382602. doi 10.1002/ana.24096
Chiò, A., Logroscino, G., and Hardiman, O., Prognostic factors in ALS: A critical review, Amyotrophic Lateral Scler., 2009, vol. 10, nos. 5–6, pp. 310–323. PMID 24382602. doi 10.1002/ana.24096
Kalra, S., Vitale, A., Cashman, N.R., et al., Cerebral degeneration predicts survival in amyotrophic lateral sclerosis, J. Neurol. Neurosurg. Psychiatry, 2006, vol. 77, no. 11, pp. 1253–1255. PMID 16835288. doi 10.1136/jnnp.2006.090696
Pyra, T., Hui, B., Hanstock, C., et al., Combined structural and neurochemical evaluation of the corticospinal tract in amyotrophic lateral sclerosis, Amyotrophic Lateral Scler., 2010, vol. 11, nos. 1–2, pp. 157–165. PMID 19242831. doi 10.3109/ 17482960902756473
Agosta, F., Pagani, E., Petrolini, M., et al., MRI predictors of long-term evolution in amyotrophic lateral sclerosis, Eur. J. Neurosci., 2010, vol. 32, pp. 1490–1496. PMID 21044177. doi 10.1111/j.1460-9568. 2010.07445.x.
Konrad, C., Henningsen, H., Bremer, J., et al., Pattern of cortical reorganization in amyotrophic lateral sclerosis: a functional magnetic resonance imaging study, Exp. Brain Res., 2002, vol. 143, no. 1, pp. 51–56. PMID 11907690. doi 10.1007/s00221-001-0981-9
Lulé, D., Diekmann, V., Kassubek, J., et al., Cortical plasticity in amyotrophic lateral sclerosis: motor imagery and function, Neurorehabil. Neural Repair, 2007, vol. 21, no. 6, pp. 518–526. PMID 17476000. doi 10.1177/1545968307300698
Stanton, B.R., Williams, V.C., Leigh, P.N., et al., Altered cortical activation during a motor task in ALS. Evidence for involvement of central pathways, J. Neurol., 2007, vol. 254, no. 9, pp. 1260–1267. PMID 17385077. doi 10.1007/s00415-006-0513-4
Poujois, A., Schneider, F.C., Faillenot, I., et al., Brain plasticity in the motor network is correlated with disease progression in amyotrophic lateral sclerosis, Hum. Brain Mapp., 2013, vol. 34, no. 10, pp. 2391–2401. PMID 22461315. doi 10.1002/hbm.22070
Chervyakov, A.V., Bakulin, I.S., Savitskaya, N.G., et al., Navigated transcranial magnetic stimulation in amyotrophic lateral sclerosis, Muscle Nerve, 2015, vol. 51, no. 1, pp. 125–131. PMID 25049055. doi 10.1002/mus.24345
Bakulin, I.S., Chervyakov, A.V., Suponeva, N.A., et al., Motor cortex hyperexcitability, neuroplasticity and degeneration in amyotrophic lateral sclerosis, in Novel Aspects of Amyotrophic Lateral Sclerosis, Foyaca-Sibat, H., Ed., Rijeka: InTech, 2016, pp. 47–72.
Turner, M.R., Hammers, A., Al-Chalabi, A., et al., Distinct cerebral lesions in sporadic and ‘D90A’ SOD1 ALS: studies with [11C]flumazenil PET, Brain, 2005, vol. 128, no. 6, pp. 1323–1329. PMID 15843422. doi 10.1093/brain/awh509
Bede, P., Bokde, A.L., Byrne, S., et al., Multiparametric MRI study of ALS stratified for the C9orf72 genotype, Neurology, 2013, vol. 81, pp. 361–369. PMID 23771489. doi 10.1212/WNL.0b013e31829c5eee
Ng, M.C., Ho, J.T., Ho, S.L., et al., Abnormal diffusion tensor in nonsymptomatic familial amyotrophic lateral sclerosis with a causative superoxide dismutase 1 mutation, J. Magn. Reson. Imaging, 2008, vol. 27, pp. 8–13. PMID 18022844. doi 10.1002/jmri.21217
Carew, J.D., Nair, G., Andersen, P.M., et al., Presymptomatic spinal cord neurometabolic findings in SOD1-positive people at risk for familial ALS, Neurology, 2011, vol. 77, no. 14, pp. 1370–1375. PMID 21940617. doi 10.1212/WNL.0b013e318231526a
Walhout, R., Schmidt, R., Westeneng, H.J., et al., Brain morphologic changes in asymptomatic C9orf72 repeat expansion carriers, Neurology, 2015, vol. 85, no. 20, pp. 1780–1788. PMID 26497991. doi 10.1212/ WNL.0000000000002135
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Bakulin, I.S., Chervyakov, A.V., Kremneva, E.I. et al. Structural and Functional Neuroimaging in Amyotrophic Lateral Sclerosis. Hum Physiol 44, 844–854 (2018). https://doi.org/10.1134/S0362119718080029
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DOI: https://doi.org/10.1134/S0362119718080029