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Review Article

Primary lateral sclerosis: a distinct entity or part of the ALS spectrum?

, , , &
Pages 133-145 | Received 07 Oct 2018, Accepted 09 Nov 2018, Published online: 18 Jan 2019

References

  • Le Forestier N, Maisonobe T, Piquard A, Rivaud S, Crevier-Buchman L, Salachas F, et al. Does primary lateral sclerosis exist? A study of 20 patients and a review of the literature. Brain. 2001;124:1989–99.
  • Brugman F, Wokke JHJ, Vianney de Jong JMB, Franssen H, Faber CG, Van den Berg LH, et al. Primary lateral sclerosis as a phenotypic manifestation of familial ALS. Neurology. 2005;64:1778–9.
  • Almeida V, de Carvalho M, Scotto M, Pinto S, Pinto A, Ohana B, et al. Primary lateral sclerosis: predicting functional outcome. Amyotroph Lateral Scler Frontotemporal Degener. 2013;14:141–5.
  • Singer MA, Kojan S, Barohn RJ, Herbelin L, Nations SP, Trivedi JR, et al. Primary lateral sclerosis: clinical and laboratory features in 25 patients. J Clin Neuromuscul Dis. 2005;7:1–9.
  • Talman P, Forbes A, Mathers S. Clinical phenotypes and natural progression for motor neuron disease: analysis from an Australian database. Amyotroph Lateral Scler. 2009;10:79–84.
  • Pringle CE, Hudson AJ, Munoz DG, Kiernan JA, Brown WF, Ebers GC, et al. Primary lateral sclerosis. Clinical features, neuropathology and diagnostic criteria. Brain 1992;115:495–520.
  • Fournier CN, Murphy A, Loci L, Mitsumoto H, Lomen-Hoerth C, Kisanuki Y, et al. Primary lateral sclerosis and early upper motor neuron disease: characteristics of a cross-sectional population. J Clin Neuromuscul Dis. 2016;17:99–105.
  • Swash M, Desai J, Misra VP. What is primary lateral sclerosis? J Neurol Sci. 1999;170:5–10.
  • Huntsman R, Lemire E, Norton J, Dzus A, Blakley P, Hasal S, et al. The differential diagnosis of spastic diplegia. Arch Dis Child. 2015;100:500–4.
  • Strong MJ, Gordon PH. Primary lateral sclerosis, hereditary spastic paraplegia and amyotrophic lateral sclerosis: discrete entities or spectrum? Amyotroph Lateral Scler Other Motor Neuron Disord. 2005;6:8–16.
  • Gordon PH, Cheng B, Katz IB, Pinto M, Hays AP, Mitsumoto H, et al. The natural history of primary lateral sclerosis. Neurology. 2006;66:647–53.
  • D'Amico E, Pasmantier M, Lee YW, et al. Clinical evolution of pure upper motor neuron disease/dysfunction (PUMMD). Muscle Nerve. 2013;47:28–32.
  • Clark MG, Smallwood Shoukry R, Huang CJ, Danielian LE, Bageac D, Floeter MK, et al. Loss of functional connectivity is an early imaging marker in primary lateral sclerosis. Amyotroph Lateral Scler Frontotemporal Degener. 2018;9:1–8.
  • Le Forestier N, Meininger V. Primary lateral sclerosis: the era of international diagnosis criteria. Rev Neurol (Paris). 2009;165:415–29.
  • de Vries BS, Rustemeijer LMM, van der Kooi AJ, et al. A case series of PLS patients with frontotemporal dementia and overview of the literature. Amyotroph Lateral Scler Frontotemporal Degener. 2017;18:534–48.
  • Johnson K, Dimachkie M, Pasnoor M, et al. Primary lateral sclerosis plus corticobasal syndrome: a case series. Neurology. 2015;84.
  • Mills CK. A case of unilateral ascending paralysis, probably presenting a new form of degenerative disease. J Nerv Ment Dis. 1900;27:195–200.
  • Gastaut JL, Bartolomei F. Mills' syndrome: ascending (or descending) progressive hemiplegia: a hemiplegic form of primary lateral sclerosis? [10]. J Neurol Neurosurg Psychiatr. 1994;57:1280–1.
  • Maragakis NJ, Holland NR, Corse AM. Hemiparetic primary lateral sclerosis: revisiting mills syndrome. Case Rep Neurol. 2013;7:191–5.
  • Ekmekci H, Ozturk S, Demir A. Mills' syndrome: a case report. Eur J Neurol. 2011;18:619.
  • Turner MR, Gerhard A, Al-Chalabi A, et al. Mills' and other isolated upper motor neurone syndromes: in vivo study with 11C-(R)-PK11195 PET. J Neurol, Neurosurger Psychiatr. 2005;76:871–4.
  • Van Laere K, Wilms G, Van Damme P. FDG-PET findings in three cases of Mills' syndrome. J Neurol, Neurosurg Psychiatr. 2016;87:222–3.
  • Tartaglia MC, Rowe A, Findlater K, Orange JB, Grace G, Strong MJ, et al. Differentiation between primary lateral sclerosis and amyotrophic lateral sclerosis: examination of symptoms and signs at disease onset and during follow-up. Arch Neurol. 2007;64:232–6.
  • Floeter MK, Mills R. Progression in primary lateral sclerosis: a prospective analysis. Amyotroph Lateral Scler. 2009;10:339–46.
  • Bede P, Querin G, Pradat PF. The changing landscape of motor neuron disease imaging: the transition from descriptive studies to precision clinical tools. Curr Opin Neurol. 2018;31:431–8.
  • Charil A, Corbo M, Filippi M, Kesavadas C, Agosta F, Munerati E, et al. Structural and metabolic changes in the brain of patients with upper motor neuron disorders: a multiparametric MRI study. Amyotroph Lateral Scler. 2009;10:269–79.
  • Paganoni S, Alshikho MJ, Zürcher NR, Cernasov P, Babu S, Loggia ML, et al. Imaging of glia activation in people with primary lateral sclerosis. NeuroImage: Clin. 2018;17:347–53.
  • Amber Dale A, Abdennadher M, Mouti M, et al. A case of progressive asymmetric limb weakness with abnormal fluorodeoxyglucose (FDG)-positron emission tomography (PET). J Clin Neuromuscul Dis. 2017;18:S13.
  • Scialò C, Morbelli S, Girtler N, Mandich P, Mancardi GL, Caponnetto C, et al. Bilateral motor and premotor cortex hypometabolism in a case of Mills syndrome. Amyotroph Lateral Scler Frontotemporal Degener. 2015;16:414–7.
  • Arruda WO, Coelho Neto M. Primary lateral sclerosis. A case report with SPECT study. Arq Neuropsiquiatr. 1998;56:465–71.
  • Van Laere K, Vanhee A, Verschueren J, De Coster L, Driesen A, Dupont P, et al. Value of 18fluorodeoxyglucose-positron-emission tomography in amyotrophic lateral sclerosis: a prospective study. JAMA Neurol. 2014;71:553–61.
  • Marti-Fabregas J, Pujol J. Selective involvement of the pyramidal tract on magnetic resonance imaging in primary lateral sclerosis. Neurology. 1990;40:1799–800.
  • Budrewicz S, Szewczyk P, Slotwinski K, et al. Symptoms of degeneration of the pyramidal tracts in conventional magnetic resonance imaging and diffusion tensor imaging in a young woman with primary lateral sclerosis. J Postgrad Med. 2015;61:206–8.
  • Lindenberg J, Preston DC. MRI imaging in primary lateral sclerosis. J Clin Neuromuscul Dis. 2003;4:115–6.
  • Mascalchi M, F, Salvi F, Valzania, et al. Corticospinal tract degeneration in motor neuron disease. Am J Neuroradiol. 1995;16:878–80.
  • Bede P, Bokde ALW, Byrne S, Elamin M, Fagan AJ, Hardiman O, et al. Spinal cord markers in ALS: diagnostic and biomarker considerations. Amyotroph Lateral Scler. 2012;13:407–15.
  • Jimenez-Caballero PE, Alvarez-Tejerina A. Degeneration of the corticospinal pathway in primary lateral sclerosis. Revista de Neurologia. 2003;36:898.
  • Paliwal VK, Rahi SK, Singh P, Gupta RK. "Wine-glass appearance" of pyramidal tracts in a patient with primary lateral sclerosis. Neurol India. 2012;60:110–1.
  • Smith CD. Serial MRI findings in a case of primary lateral sclerosis. Neurology. 2002;58:647–9.
  • Tzarouchi LC, Kyritsis AP, Giannopoulos S, Astrakas LG, Diakou M, Argyropoulou MI, et al. Voxel-based diffusion tensor imaging detects pyramidal tract degeneration in primary lateral sclerosis. Bjr. 2011;84:78–80.
  • Suh SI, Song IC, Koh SB. Primary lateral sclerosis with MR diffusion tensor image and tract tracking. Am J Phys Med Rehabil. 2006;85:863–4.
  • Salameh JS, Patel N, Zheng S, Cauley KA. Focal absence of diffusion tensor tracts from primary motor cortex in primary lateral sclerosis. Eur J Neurol. 2013;20:e63–4.
  • Bede P, Elamin M, Byrne S, McLaughlin RL, Kenna K, Vajda A, et al. Patterns of cerebral and cerebellar white matter degeneration in ALS. J Neurol Neurosurg Psychiatr. 2015;86:468–70.
  • Tartaglia MC, Laluz V, Rowe A, Findlater K, Lee DH, Kennedy K, et al. Brain atrophy in primary lateral sclerosis. Neurology. 2009;72:1236–41.
  • van der Graaff MM, Sage CA, Caan MWA, Akkerman EM, Lavini C, Majoie CB, et al. Upper and extra-motoneuron involvement in early motoneuron disease: a diffusion tensor imaging study. Brain. 2011;134:1211–28.
  • Kiernan JA, Hudson AJ. Frontal lobe atrophy in motor neuron diseases. Brain. 1994;117:747–57.
  • Kuipers-Upmeijer J, de Jager AE, Hew JM, et al. Primary lateral sclerosis: clinical, neurophysiological, and magnetic resonance findings. J Neurol Neurosurg Psychiatr. 2001;71:615–20.
  • Schuster C, Kasper E, Machts J, Bittner D, Kaufmann J, Benecke R, et al. Focal thinning of the motor cortex mirrors clinical features of amyotrophic lateral sclerosis and their phenotypes: a neuroimaging study. J Neurol. 2013;260:2856–64.
  • Butman JA, Floeter MK. Decreased thickness of primary motor cortex in primary lateral sclerosis. Am J Neuroradiol. 2007;28:87–91.
  • Ulug AM, Grunewald T, Lin MT, et al. Diffusion tensor imaging in the diagnosis of primary lateral sclerosis. J Magn Reson Imaging. 2004;19:34–9.
  • Ciccarelli O, Behrens TE, Johansen-Berg H, Talbot K, Orrell RW, Howard RS, et al. Investigation of white matter pathology in ALS and PLS using tract-based spatial statistics. Hum Brain Mapp. 2009;30:615–24.
  • Iwata NK, Kwan JY, Danielian LE, Butman JA, Tovar-Moll F, Bayat E, et al. White matter alterations differ in primary lateral sclerosis and amyotrophic lateral sclerosis. Brain. 2011;134:2642–55.
  • Agosta F, Galantucci S, Riva N, Chiò A, Messina S, Iannaccone S, et al. Intrahemispheric and interhemispheric structural network abnormalities in PLS and ALS. Hum Brain Mapp. 2014;35:1710–22.
  • Unrath A, Mueller HP, Riecker A, et al. Whole brain-based multiparametric MRI analysis of regional white matter tract alterations in rare motor neuron diseases by diffusion tensor imaging. Klinische Neurophysiologie 2010;41:1727-40.
  • Müller H-P, Unrath A, Huppertz H-J, Ludolph AC, Kassubek J. Neuroanatomical patterns of cerebral white matter involvement in different motor neuron diseases as studied by diffusion tensor imaging analysis. Amyotroph Lateral Scler. 2012;13:254–64.
  • Chan S, Shungu DC, Douglas-Akinwande A, Lange DJ, Rowland LP. Motor neuron diseases: comparison of single-voxel proton MR spectroscopy of the motor cortex with MR imaging of the brain. Radiology. 1999;212:763–9.
  • Zhai P, Pagan F, Statland J, Butman JA, Floeter MK. Primary lateral sclerosis: a heterogeneous disorder composed of different subtypes? Neurology. 2003;60:1258–65.
  • Mitsumoto H, Ulug AM, Pullman SL, Gooch CL, Chan S, Tang M-X, et al. Quantitative objective markers for upper and lower motor neuron dysfunction in ALS. Neurology. 2007;68:1402–10.
  • van der Graaff MM, Lavini C, Akkerman EM, Majoie CB, Nederveen AJ, Zwinderman AH, et al. MR spectroscopy findings in early stages of motor neuron disease. Am J Neuroradiol. 2010;31:1799–806.
  • Agosta F, Canu E, Inuggi A, Chiò A, Riva N, Silani V, et al. Resting state functional connectivity alterations in primary lateral sclerosis. Neurobiol Aging. 2014;35:916–25.
  • Meoded A, Morrissette AE, Katipally R, Schanz O, Gotts SJ, Floeter MK, et al. Cerebro-cerebellar connectivity is increased in primary lateral sclerosis. NeuroImage Clin. 2015;7:288–96.
  • Querin G, El Mendili MM, Bede P, et al. Multimodal spinal cord MRI offers accurate diagnostic classification in ALS. J Neurol Neurosurg Psychiatr. 2018;89:1220-21.
  • Mitsumoto H, PL, Nagy C, Gennings , et al. Phenotypic and molecular analyses of primary lateral sclerosis. Neurol Genet. 2015;1:e3. doi:10.1212/01.NXG.0000464294.88607.dd
  • Kwan JY, Meoded A, Danielian LE, Wu T, Floeter MK. Structural imaging differences and longitudinal changes in primary lateral sclerosis and amyotrophic lateral sclerosis. NeuroImage: Clin. 2013;2:151–60.
  • Fabes J, Matthews L, Filippini N, Talbot K, Jenkinson M, Turner MR, et al. Quantitative FLAIR MRI in amyotrophic lateral sclerosis. Acad Radiol. 2017;24:1187–94.
  • Kolind S, Sharma R, Knight S, Johansen-Berg H, Talbot K, Turner MR, et al. Myelin imaging in amyotrophic and primary lateral sclerosis. Amyotroph Lateral Scler Frontotemporal Degener. 2013;14:562–73.
  • Schuster C, Elamin M, Hardiman O, Bede P. Presymptomatic and longitudinal neuroimaging in neurodegeneration–from snapshots to motion picture: a systematic review. J Neurol Neurosurg Psychiatry. 2015;86:1089–96.
  • Bede P, Hardiman O. Longitudinal structural changes in ALS: a three time-point imaging study of white and gray matter degeneration. Amyotroph Lateral Scler Frontotemporal Degener. 2018;19:232–41.
  • Menke RAL, Abraham I, Thiel CS, Filippini N, Knight S, Talbot K, et al. Fractional anisotropy in the posterior limb of the internal capsule and prognosis in amyotrophic lateral sclerosis. Arch Neurol. 2012;69:1493–9.
  • Machts J, Cardenas-Blanco A, Acosta-Cabronero J, Kaufmann J, Loewe K, Kasper E, et al. Prefrontal cortical thickness in motor neuron disease. NeuroImage: Clin. 2018;18:648–55.
  • Menke RAL, Proudfoot M, Talbot K, Turner MR. The two-year progression of structural and functional cerebral MRI in amyotrophic lateral sclerosis. NeuroImage: Clin. 2018;17:953–61.
  • Ferraro PM, Agosta F, Riva N, Copetti M, Spinelli EG, Falzone Y, et al. Multimodal structural MRI in the diagnosis of motor neuron diseases. NeuroImage Clin. 2017;16:240–7.
  • Müller H-P, Gorges M, Kassubek R, Dorst J, Ludolph AC, Kassubek J, et al. Identical patterns of cortico-efferent tract involvement in primary lateral sclerosis and amyotrophic lateral sclerosis: a tract of interest-based MRI study. NeuroImage: Clin. 2018;18:762–9.
  • Bede P, Hardiman O. Lessons of ALS imaging: pitfalls and future directions - A critical review. Neuroimage Clin. 2014;4:436–43.
  • Turner MR, Hammers A, Al-Chalabi A, Shaw CE, Andersen PM, Brooks DJ, et al. Cortical involvement in four cases of primary lateral sclerosis using [11C]-flumazenil PET. J Neurol. 2007;254:1033–6.
  • Van Weehaeghe D, Ceccarini J, Delva A, Robberecht W, Van Damme P, Van Laere K, et al. Prospective validation of 18F-FDG brain PET discriminant analysis methods in the diagnosis of amyotrophic lateral sclerosis. J Nuclear Med. 2016;57:1238–43.
  • Fisher CM. Pure spastic paralysis of corticospinal origin. Can J Neurol Sci. 1977;4:251–8.
  • Younger DS, Chou S, Hays AP, et al. Primary lateral sclerosis. A clinical diagnosis reemerges. Arch Neurol. 1988;45:1304–7.
  • Sugihara H, Horiuchi M, Kamo T, Fujisawa K, Abe M, Sakiyama T, et al. A case of primary lateral sclerosis taking a prolonged clinical course with dementia and having an unusual dendritic ballooning. Neuropathol. 1999;19:77–84.
  • Tan CF, Kakita A, Piao YS, et al. Primary lateral sclerosis: a rare upper-motor-predominant form of amyotrophic lateral sclerosis often accompanied by frontotemporal lobar degeneration with ubiquitinated neuronal inclusions? Report of an autopsy case and a review of the literature. Acta Neuropathologica. 2003;105:615–20.
  • Engel PA, Grunnet M. Atypical dementia and spastic paraplegia in a patient with primary lateral sclerosis and numerous necortical beta amyloid plaques: new disorder or Alzheimer's disease variant? J Geriatr Psychiatry Neurol. 2000;13:60–4.
  • Smith MC. Nerve fibre degeneration in the brain in amiotrophyc lateral sclerosis. J Neurol Neurosurg Psychiatr. 1960;23:269–82.
  • Saberi S, Stauffer JE, Schulte DJ, Ravits J. Neuropathology of amyotrophic lateral sclerosis and its variants. Neurologic Clin. 2015;33:855–76.
  • Singer MA, Statland JM, Wolfe GI, Barohn RJ. Primary lateral sclerosis. Muscle Nerve. 2007;35:291–302.
  • Bunina TL. On intracellular inclusions in familial amyotrophic lateral sclerosis. Zh Nevropatol Psikhiatr Im S S Korsakova 1962;62:1293–9.
  • Beal MF, Richardson EP. Jr.. Primary lateral sclerosis: a case report. Arch Neurol. 1981;38:630–3.
  • Kosaka T, Fu Y-J, Shiga A, Ishidaira H, Tan C-F, Tani T, et al. Primary lateral sclerosis: upper-motor-predominant amyotrophic lateral sclerosis with frontotemporal lobar degeneration–immunohistochemical and biochemical analyses of TDP-43. Neuropathology. 2012;32:373–84.
  • Imai H, Furukawa Y, Sumino S, et al. A 65-year-old woman with dysarthria, dysphagia, weakness, and gait disturbance. Brain Nerve. 1995;47:399–410.
  • Hudson AJ, Kiernan JA, Munoz DG, Pringle CE, Brown WF, Ebers GC, et al. Clinicopathological features of primary lateral sclerosis are different from amyotrophic lateral sclerosis. Brain Res Bulletin. 1993;30:359–64.
  • Watanabe R, Iino M, Honda M, Sano J, Hara M. Primary lateral sclerosis. Neuropathol. 1997;17:220–4.
  • Leigh PN, Anderton BH, Dodson A, Gallo JM, Swash M, Power DM, et al. Ubiquitin deposits in anterior horn cells in motor neurone disease. Neurosci Lett. 1988;93:197–203.
  • Lowe J, Lennox G, Jefferson D, Morrell K, McQuire D, Gray T, et al. A filamentous inclusion body within anterior horn neurones in motor neurone disease defined by immunocytochemical localisation of ubiquitin. Neurosci Lett. 1988;94:203–10.
  • Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science. 2006;314:130–3.
  • Lu JQ, Carter J, Johnston W. Primary lateral sclerosis without TDP-43 pathology: a case study. J Neuropathol Exper Neurol. 2010;69:533–4.
  • Dickson DW, Josephs KA, Amador-Ortiz C. TDP-43 in differential diagnosis of motor neuron disorders. Acta Neuropathol. 2007;114:71–9.
  • Brettschneider J, Del Tredici K, Toledo JB, Robinson JL, Irwin DJ, Grossman M, et al. Stages of pTDP-43 pathology in amyotrophic lateral sclerosis. Ann Neurol. 2013;74:20–38.
  • Kassubek J, Muller H-P, Del Tredici K, Brettschneider J, Pinkhardt EH, Lule D, et al. Diffusion tensor imaging analysis of sequential spreading of disease in amyotrophic lateral sclerosis confirms patterns of TDP-43 pathology. Brain. 2014;137:1733–40.
  • Konagaya M, Sakai M, Iida M, et al. An autopsied case of dominantly affecting upper motor neuron with atrophy of the frontal and temporal lobes. With special reference to primary lateral sclerosis. Clin Neurol. 1995;35:384–90.
  • Tsuchiya K, Arai M, Matsuya S, Nishimura H, Ishiko T, Kondo H, et al. Sporadic amyotrophic lateral sclerosis resembling primary lateral sclerosis: report of an autopsy case and a review of the literature. Neuropathology. 1999;19:71–6.
  • Mackenzie IR, Feldman H. Neurofilament inclusion body disease with early onset frontotemporal dementia and primary lateral sclerosis. Clin Neuropathol. 2004;23:183–93.
  • Short CL, Scott G, Blumbergs PC, et al. A case of presumptive primary lateral sclerosis with upper and lower motor neurone pathology. J Clin Neurosci. 2005;12:708–9.
  • Kobayashi Z, Tsuchiya K, Arai T, Yokota O, Yoshida M, Shimomura Y, et al. Clinicopathological characteristics of FTLD-TDP showing corticospinal tract degeneration but lacking lower motor neuron loss. J Neurol Sci. 2010;298:70–7.
  • Mochizuki A, Komatsuzaki Y, Iwamoto H, Shoji S. Frontotemporal dementia with ubiquitinated neuronal inclusions presenting with primary lateral sclerosis and parkinsonism: clinicopathological report of an autopsy case. Acta Neuropathol. 2004;107:377–80.
  • Josephs K, Whitwell J, Murray M, et al. Semantic dementia with primary lateral sclerosis (SD-PLS): a variant of FTLD-TDP type C pathology. Dementia Geriatric Cognitive Dis. 2012;34:37–8.
  • Kawakatsu S, Kobayashi R, Shibuya Y, et al. A case of FTLD-TDP type a with primary lateral sclerosis presenting progressive nonfluent aphasia, anterior operculum syndrome and left pyramidal tract lesion on MRI. Neuropathology. 2013;33:364.
  • Antunes A, Pinto S, Almeida V, et al. Heterogeneity in familial motor neuron disease. J Neurol. 2011;258:S81–S2.
  • Praline J, Guennoc A-M, Vourc'h P, De Toffol B, Corcia P. Primary lateral sclerosis may occur within familial amyotrophic lateral sclerosis pedigrees. Amyotroph Lateral Scler. 2010;11:154–6.
  • van Rheenen W, van Blitterswijk M, Huisman MHB, Vlam L, van Doormaal PTC, Seelen M, et al. Hexanucleotide repeat expansions in C9ORF72 in the spectrum of motor neuron diseases. Neurology. 2012;79:878–82.
  • Sanchez-Ferrero E, Coto E, Beetz C, et al. SPG7 mutational screening in spastic paraplegia patients supports a dominant effect for some mutations and a pathogenic role for p.A510V. Clin Genet. 2013;83:257–62.
  • Yang Y, L, Zhang DR, Lynch , et al. Compound heterozygote mutations in SPG7 in a family with adult-onset primary lateral sclerosis. Neurol Gen. 2016;2:e60.
  • Gomez-Tortosa E, Van der Zee J, Ruggiero M, et al. Familial primary lateral sclerosis or dementia associated with Arg573Gly TBK1 mutation. J Neurol Neurosurg Psychiatr. 2017;88:996-7.
  • Brugman F, Veldink JH, Franssen H, et al. Differentiation of hereditary spastic paraparesis from primary lateral sclerosis in sporadic adult-onset upper motor neuron syndromes. Arch Neurol. 2009;66:509–14.
  • Dupre N, Valdmanis PN, Bouchard J-P, Rouleau GA. Autosomal dominant primary lateral sclerosis. Neurology. 2007;68:1156–7.
  • Steinacker P, Feneberg E, Weishaupt J, et al. Neurofilaments in the diagnosis of motoneuron diseases: a prospective study on 455 patients. J Neurol Neurosurger Psychiatr. 2016;87:12–20.
  • Thompson AG, Gray E, Thézénas M-L, Charles PD, Evetts S, Hu MT, et al. Cerebrospinal fluid macrophage biomarkers in amyotrophic lateral sclerosis. Ann Neurol. 2018;83:258–68.
  • Agarwal S, Koch G, Hillis AE, et al. Interrogating cortical function with transcranial magnetic stimulation: insights from neurodegenerative disease and stroke. J Neurol Neurosurg Psychiatr. 2018;pii: jnnp-2017-317371. doi: 10.1136/jnnp-2017-317371. [Epub ahead of print].
  • Mills KR, Nithi KA. Corticomotor threshold is reduced in early sporadic amyotrophic lateral sclerosis. Muscle Nerve. 1997;20:1137–41.
  • Vucic S, Kiernan MC. Novel threshold tracking techniques suggest that cortical hyperexcitability is an early feature of motor neuron disease. Brain. 2006;129:2436–46.
  • Cruz Martinez A, Trejo JM. Transcranial magnetic stimulation in amyotrophic and primary lateral sclerosis. Electromyograph Clin Neurophysiol. 1999;39:285–8.
  • Fisher KM, Zaaimi B, Williams TL, Baker SN, Baker MR. Beta-band intermuscular coherence: a novel biomarker of upper motor neuron dysfunction in motor neuron disease. Brain. 2012;135:2849–64.
  • Proudfoot M, Rohenkohl G, Quinn A, Colclough GL, Wuu J, Talbot K, et al. Altered cortical beta-band oscillations reflect motor system degeneration in amyotrophic lateral sclerosis. Hum Brain Mapp. 2017;38:237–54.
  • Agarwal S, Highton-Williamson E, Caga J, Matamala JM, Dharmadasa T, Howells J, et al. Primary lateral sclerosis and the amyotrophic lateral sclerosis-frontotemporal dementia spectrum. J Neurol. 2018;265:1819–28.
  • Brooks BR, Miller RG, Swash M, Munsat TL. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Dis. 2000;1:293–9.
  • McHale B, Hupf J, Ibagon C, et al. The aim and development of the primary lateral sclerosis functional rating scale (PLSFRS). Amyotroph Lateral Scler Frontotemporal Degener. 2017;18:271–2.
  • Bede P, Elamin M, Byrne S, et al. Sexual dimorphism in ALS: exploring gender-specific neuroimaging signatures. Amyotroph Lateral Scler Frontotemporal Degener. 2013;15:235-43.
  • Bede P, Omer T, Finegan E, et al. Connectivity-based characterisation of subcortical grey matter pathology in frontotemporal dementia and ALS: a multimodal neuroimaging study. Brain Imaging Behav. 2018. doi: 10.1007/s11682-018-9837-9. [Epub ahead of print].
  • Bede P, Iyer PM, Finegan E, Omer T, Hardiman O. Virtual brain biopsies in amyotrophic lateral sclerosis: Diagnostic classification based on in vivo pathological patterns. Neuroimage Clin. 2017;15:653–8.
  • Schuster C, Hardiman O, Bede P. Survival prediction in Amyotrophic lateral sclerosis based on MRI measures and clinical characteristics. BMC Neurol. 2017;17:73.
  • Muller HP, Turner MR, Grosskreutz J, et al. A large-scale multicentre cerebral diffusion tensor imaging study in amyotrophic lateral sclerosis. J Neurol Neurosurg Psychiatry. 2016;87:570–9.

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