MRI biomarkers for memory-related impairment in amyotrophic lateral sclerosis: a systematic review

References

• Morrow JM, Sinclair CDJ, Fischmann A, Machado PM, Reilly MM, Yousry TA, et al. MRI biomarker assessment of neuromuscular disease progression: a prospective observational cohort study. Lancet Neurol. 2016;15:65–77.
   PubMed Web of Science ®Google Scholar
• Carlier PG, Reyngoudt H. The expanding role of MRI in neuromuscular disorders. Nat Rev Neurol. 2020;16:301–2.
   PubMed Web of Science ®Google Scholar
• Müller M, Dohrn MF, Romanzetti S, Gadermayr M, Reetz K, Krämer NA, et al. Semi-automated volumetry of MRI serves as a biomarker in neuromuscular patients. Muscle Nerve. 2020;61:600–7.
   PubMed Web of Science ®Google Scholar
• Dahlqvist JR, Widholm P, Leinhard OD, Vissing J. MRI in neuromuscular diseases: an emerging diagnostic tool and biomarker for prognosis and efficacy. Ann Neurol. 2020;88:669–81.
   PubMed Web of Science ®Google Scholar
• Behler A, Müller HP, Ludolph AC, Kassubek J. Diffusion tensor imaging in amyotrophic lateral sclerosis: machine learning for biomarker development. Int J Mol Sci 2023;24:1911.
   PubMed Web of Science ®Google Scholar
• Ghaderi S, Olfati M, Ghaderi M, Hadizadeh H, Yazdanpanah G, Khodadadi Z, et al. Neurological manifestation in COVID-19 disease with neuroimaging studies. Am J Neurodegener Dis 2023;12:42–84.
   PubMedGoogle Scholar
• Yang T, Tian S, Li Y, Tian X, Wang W, Zhao J, et al. Magnetic resonance imaging (MRI) and three-dimensional transvaginal ultrasonography scanning for preoperative assessment of high risk in women with endometrial cancer. Med Sci Monit. 2019;25:2024–31.
   PubMed Web of Science ®Google Scholar
• Bayram E, Caldwell JZK, Banks SJ. Current understanding of magnetic resonance imaging biomarkers and memory in Alzheimer’s disease. Alzheimers Dement. 2018;4:395–413.
   Google Scholar
• Bhattarai A, Egan GF, Talman P, Chua P, Chen Z. Magnetic resonance iron imaging in amyotrophic lateral sclerosis. J Magn Reson Imaging. 2022;55:1283–300.
   PubMed Web of Science ®Google Scholar
• Paoletti M, Diamanti L, Muzic SI, Ballante E, Solazzo F, Foppoli L, et al. Longitudinal quantitative MRI evaluation of muscle involvement in amyotrophic lateral sclerosis. Front Neurol. 2021;12:749736.
   PubMed Web of Science ®Google Scholar
• Bharti K,J, Graham S, Benatar M, Briemberg H, Chenji S, Dupré N, et al. Functional alterations in large-scale resting-state networks of amyotrophic lateral sclerosis: a multi-site study across Canada and the United States. PLOS One. 2022;17:e0269154.
   PubMed Web of Science ®Google Scholar
• Papps B, Abrahams S, Wicks P, Leigh PN, Goldstein LH. Changes in memory for emotional material in amyotrophic lateral sclerosis (ALS). Neuropsychologia 2005;43:1107–14.
   PubMed Web of Science ®Google Scholar
• Zarei S, Carr K, Reiley L, Diaz K, Guerra O, Altamirano PF, et al. A comprehensive review of amyotrophic lateral sclerosis. Surg Neurol Int. 2015;6:171.
   PubMedGoogle Scholar
• Talbot K. Motor neurone disease. Postgrad Med J. 2002;78:513–9.
   PubMed Web of Science ®Google Scholar
• Savage AL, Iacoangeli A, Schumann GG, Rubio-Roldan A, Garcia-Perez JL, Al Khleifat A, et al. Characterisation of retrotransposon insertion polymorphisms in whole genome sequencing data from individuals with amyotrophic lateral sclerosis. Gene 2022;843:146799.
   PubMed Web of Science ®Google Scholar
• Temp AGM, Kasper E, Machts J, Vielhaber S, Teipel S, Hermann A, et al. Cognitive reserve protects ALS‐typical cognitive domains: a longitudinal study. Ann Clin Transl Neurol. 2022;9:1212–23.
   PubMed Web of Science ®Google Scholar
• Machts J, Keute M, Kaufmann J, Schreiber S, Kasper E, Petri S, et al. Longitudinal clinical and neuroanatomical correlates of memory impairment in motor neuron disease. Neuroimage Clin. 2021;29:102545.
   PubMed Web of Science ®Google Scholar
• El Mendili MM, Grapperon AM, Dintrich R, Stellmann JP, Ranjeva JP, Guye M, et al. Alterations of microstructure and sodium homeostasis in fast amyotrophic lateral sclerosis progressors: a brain DTI and sodium MRI study. AJNR Am J Neuroradiol. 2022;43:984–90.
   PubMedGoogle Scholar
• Ahmad L, Zhang SY, Casanova JL, Sancho-Shimizu V. Human TBK1: a gatekeeper of neuroinflammation. Trends Mol Med. 2016;22:511–27.
   PubMed Web of Science ®Google Scholar
• Ferrari R, Kapogiannis D, Huey ED, Momeni P. FTD and ALS: a tale of two diseases. Curr Alzheimer Res. 2011;8:273–94.
   PubMed Web of Science ®Google Scholar
• Trojsi F, Di Nardo F, Caiazzo G, Siciliano M, D’Alvano G, Ferrantino T, et al. Hippocampal connectivity in amyotrophic lateral sclerosis (ALS): more than Papez circuit impairment. Brain Imaging Behav. 2021;15:2126–38.
   PubMed Web of Science ®Google Scholar
• Goldstein LH, Abrahams S. Changes in cognition and behaviour in amyotrophic lateral sclerosis: nature of impairment and implications for assessment. Lancet Neurol. 2013;12:368–80.
   PubMed Web of Science ®Google Scholar
• Neary D, Snowden J, Mann D. Frontotemporal dementia. Lancet Neurol. 2005;4:771–80.
   PubMed Web of Science ®Google Scholar
• Ahmed RM, Devenney EM, Strikwerda-Brown C, Hodges JR, Piguet O, Kiernan MC. Phenotypic variability in ALS-FTD and effect on survival. Neurology 2020;94:e2005–e2013.
   PubMed Web of Science ®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
• Masrori P, Van Damme P. Amyotrophic lateral sclerosis: a clinical review. Eur J Neurol. 2020;27:1918–29.
   PubMed Web of Science ®Google Scholar
• Montuschi A, Iazzolino B, Calvo A, Moglia C, Lopiano L, Restagno G, et al. Cognitive correlates in amyotrophic lateral sclerosis: a population-based study in Italy. J Neurol Neurosurg Psychiatry. 2015;86:168–73.
   PubMed Web of Science ®Google Scholar
• Strong MJ. The syndromes of frontotemporal dysfunction in amyotrophic lateral sclerosis. Amyotroph Lateral Scler. 2008;9:323–38.
   PubMed Web of Science ®Google Scholar
• Mojtabavi H, Nafissi S, Mahmoodi-Bakhtiari B, Fathi D, Fatehi F. Persian adaptation of edinburgh cognitive and behavioural screen (ECAS). Amyotroph Lateral Scler Frontotemporal Degener. 2021;22:426–33.
   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
• Eshghi M, Yunusova Y, Connaghan KP, Perry BJ, Maffei MF, Berry JD, et al. Rate of speech decline in individuals with amyotrophic lateral sclerosis. Sci Rep. 2022;12:15713.
   PubMed Web of Science ®Google Scholar
• Elamin M, Bede P, Byrne S, Jordan N, Gallagher L, Wynne B, et al. Cognitive changes predict functional decline in ALS: a population-based longitudinal study. Neurology 2013;80:1590–7.
   PubMed Web of Science ®Google Scholar
• Rusina R, Vandenberghe R, Bruffaerts R. Cognitive and behavioral manifestations in ALS: beyond motor system involvement. Diagnostics 2021;11:624.
   Web of Science ®Google Scholar
• Strong MJ, Abrahams S, Goldstein LH, Woolley S, Mclaughlin P, Snowden J, et al. Amyotrophic lateral sclerosis – frontotemporal spectrum disorder (ALS-FTSD): revised diagnostic criteria. Amyotroph Lateral Scler Frontotemporal Degener. 2017;18:153–74.
   PubMed Web of Science ®Google Scholar
• Hansson O. Biomarkers for neurodegenerative diseases. Nat Med. 2021;27:954–63.
   PubMed Web of Science ®Google Scholar
• Grolez G, Moreau C, Danel-Brunaud V, Delmaire C, Lopes R, Pradat PF, et al. The value of magnetic resonance imaging as a biomarker for amyotrophic lateral sclerosis: a systematic review. BMC Neurol. 2016;16:155.
   PubMed Web of Science ®Google Scholar
• Vellage AK, Veit M, Kobeleva X, Petri S, Vielhaber S, Müller NG. Working memory network changes in ALS: An fMRI study. Front Neurosci. 2016;10:158.
   PubMed Web of Science ®Google Scholar
• Machts J, Bittner V, Kasper E, Schuster C, Prudlo J, Abdulla S, et al. Memory deficits in amyotrophic lateral sclerosis are not exclusively caused by executive dysfunction: a comparative neuropsychological study of amnestic mild cognitive impairment. BMC Neurosci. 2014;15:83.
   PubMed Web of Science ®Google Scholar
• Benbrika S, Desgranges B, Eustache F, Viader F. Cognitive, emotional and psychological manifestations in amyotrophic lateral sclerosis at baseline and overtime: a review. Front Neurosci. 2019;13:951.
   PubMed Web of Science ®Google Scholar
• De Marchi F, Carrarini C, De Martino A, Diamanti L, Fasano A, Lupica A, et al. Cognitive dysfunction in amyotrophic lateral sclerosis: can we predict it? Neurol Sci. 2021;42:2211–22.
   PubMed Web of Science ®Google Scholar
• Sisakhti M, Sachdev PS, Batouli SAH. The effect of cognitive load on the retrieval of long-term memory: an FMRI study. Front Hum Neurosci. 2021;15:700146.
   PubMed Web of Science ®Google Scholar
• Seyed Amir Hossein Batouli, Sisakhti M. Investigating a hypothesis on the mechanism of long-term memory storage. Neuroquantology. 2019;17:60–80.
   Google Scholar
• Batouli SAH, Alemi R, Khoshkhouy Delshad H, Oghabian MA. The influence of mental fatigue on the face and word encoding activations. Clin Neurol Neurosurg. 2020;189:105626.
   PubMed Web of Science ®Google Scholar
• Teleanu RI, Niculescu AG, Roza E, Vladâcenco O, Grumezescu AM, Teleanu DM. Neurotransmitters—key factors in neurological and neurodegenerative disorders of the central nervous system. Int J Mol Sci 2022;23:5954.
   PubMed Web of Science ®Google Scholar
• Weerasinghe-Mudiyanselage PDE, Ang MJ, Kang S, Kim JS, Moon C. Structural plasticity of the hippocampus in neurodegenerative diseases. Int J Mol Sci. 2022;23:3349.
   PubMed Web of Science ®Google Scholar
• Gulino R. Synaptic dysfunction and plasticity in amyotrophic lateral sclerosis. Int J Mol Sci 2023;24:4613.
   PubMed Web of Science ®Google Scholar
• Arseni D, Hasegawa M, Murzin AG, Kametani F, Arai M, Yoshida M, et al. Structure of pathological TDP-43 filaments from ALS with FTLD. Nature 2022;601:139–43.
   PubMed Web of Science ®Google Scholar
• Christidi F, Karavasilis E, Velonakis G, Ferentinos P, Rentzos M, Kelekis N, et al. The clinical and radiological spectrum of hippocampal pathology in amyotrophic lateral sclerosis. Front Neurol. 2018;9:523.
   PubMed Web of Science ®Google Scholar
• Ahmed RM, Bocchetta M, Todd EG, Tse NY, Devenney EM, Tu S, et al. Tackling clinical heterogeneity across the amyotrophic lateral sclerosis–frontotemporal dementia spectrum using a transdiagnostic approach. Brain Commun. 2021;3:fcab257.
   PubMedGoogle Scholar
• Eshima J, O’Connor SA, Marschall E, Bowser R, Plaisier CL, Smith BS. Molecular subtypes of ALS are associated with differences in patient prognosis. Nat Commun. 2023;14:95.
   PubMed Web of Science ®Google Scholar
• Nie J, Zhang Z, Wang B, Li H, Xu J, Wu S, et al. Different memory patterns of digits: a functional MRI study. J Biomed Sci. 2019;26:22.
   PubMed Web of Science ®Google Scholar
• Lichtenstein T, Sprenger A, Weiss K, Große Hokamp N, Maintz D, Schlamann M, et al. MRI DTI and PDFF as biomarkers for lower motor neuron degeneration in ALS. Front Neurosci. 2021;15:682126.
   PubMed Web of Science ®Google Scholar
• Turner MR, Bowser R, Bruijn L, Dupuis L, Ludolph A, McGrath M, et al. Mechanisms, models and biomarkers in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Frontotemporal Degener. 2013; 14:19–32.
   PubMed Web of Science ®Google Scholar
• Bowser R, Cudkowicz M, Kaddurah-Daouk R. Biomarkers for amyotrophic lateral sclerosis. Expert Rev Mol Diagn. 2006;6:387–98.
   PubMed Web of Science ®Google Scholar
• Moher D, Shamseer L, Clarke M, Ghersi D, Liberati A, Petticrew M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev. 2015;4:1.
   PubMed Web of Science ®Google Scholar
• Christidi F, Argyropoulos GD, Karavasilis E, Velonakis G, Zouvelou V, Kourtesis P, et al. Hippocampal metabolic alterations in amyotrophic lateral sclerosis: a magnetic resonance spectroscopy study. Life. 2023;13:571.
   PubMedGoogle Scholar
• Kobeleva X, Machts J, Veit M, Vielhaber S, Petri S, Schoenfeld MA. Brain activity is contingent on neuropsychological function in a functional magnetic resonance imaging study of verbal working memory in amyotrophic lateral sclerosis. Eur J Neurol. 2021;28:3051–60.
   PubMed Web of Science ®Google Scholar
• Lulé DE, Müller HP, Finsel J, Weydt P, Knehr A, Winroth I, et al. Deficits in verbal fluency in presymptomatic C9orf72 mutation gene carriers-a developmental disorder. J Neurol Neurosurg Psychiatry. 2020;91:1195–200.
   PubMed Web of Science ®Google Scholar
• Chipika RH, Christidi F, Finegan E, Li Hi Shing S, McKenna MC, Chang KM, et al. Amygdala pathology in amyotrophic lateral sclerosis and primary lateral sclerosis. J Neurol Sci. 2020;417:117039.
   PubMed Web of Science ®Google Scholar
• Consonni M, Dalla Bella E, Contarino VE, Bersano E, Lauria G. Cortical thinning trajectories across disease stages and cognitive impairment in amyotrophic lateral sclerosis. Cortex. 2020;131:284–94.
   PubMed Web of Science ®Google Scholar
• Christidi F, Karavasilis E, Rentzos M, Velonakis G, Zouvelou V, Xirou S, et al. Hippocampal pathology in amyotrophic lateral sclerosis: selective vulnerability of subfields and their associated projections. Neurobiol Aging. 2019;84:178–88.
   PubMed Web of Science ®Google Scholar
• Trojsi F, Caiazzo G, Siciliano M, Femiano C, Passaniti C, Russo A, et al. Microstructural correlates of edinburgh cognitive and behavioural ALS screen (ECAS) changes in amyotrophic lateral sclerosis. Psychiatry Res Neuroimaging. 2019;288:67–75.
   PubMed Web of Science ®Google Scholar
• Bueno APA, Pinaya WHL, Moura LM, Bertoux M, Radakovic R, Kiernan MC, et al. Structural and functional papez circuit integrity in amyotrophic lateral sclerosis. Brain Imaging Behav. 2018;12:1622–30.
   PubMed Web of Science ®Google Scholar
• Lulé D, Böhm S, Müller HP, Aho-Özhan H, Keller J, Gorges M, et al. Cognitive phenotypes of sequential staging in amyotrophic lateral sclerosis. Cortex. 2018;101:163–71.
   PubMed Web of Science ®Google Scholar
• Christidi F, Karavasilis E, Zalonis I, Ferentinos P, Giavri Z, Wilde EA, et al. Memory-related white matter tract integrity in amyotrophic lateral sclerosis: an advanced neuroimaging and neuropsychological study. Neurobiol Aging. 2017;49:69–78.
   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
• Steinbach R, Loewe K, Kaufmann J, Machts J, Kollewe K, Petri S, et al. Structural hallmarks of amyotrophic lateral sclerosis progression revealed by probabilistic fiber tractography. J Neurol. 2015;262:2257–70.
   PubMed Web of Science ®Google Scholar
• Stoppel CM, Vielhaber S, Eckart C, Machts J, Kaufmann J, Heinze HJ, et al. Structural and functional hallmarks of amyotrophic lateral sclerosis progression in motor- and memory-related brain regions. Neuroimage Clin. 2014;5:277–90.
   PubMed Web of Science ®Google Scholar
• Kasper E, Schuster C, Machts J, Kaufmann J, Bittner D, Vielhaber S, et al. Microstructural white matter changes underlying cognitive and behavioural impairment in ALS–an in vivo study using DTI. PLOS One. 2014;9:e114543.
   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
• Christidi F, Zalonis I, Kyriazi S, Rentzos M, Karavasilis E, Wilde EA, et al. Uncinate fasciculus microstructure and verbal episodic memory in amyotrophic lateral sclerosis: a diffusion tensor imaging and neuropsychological study. Brain Imaging Behav. 2014;8:497–505.
   PubMed Web of Science ®Google Scholar
• Libon DJ, McMillan C, Avants B, Boller A, Morgan B, Burkholder L, et al. Deficits in concept formation in amyotrophic lateral sclerosis. Neuropsychology 2012;26:422–9.
   PubMed Web of Science ®Google Scholar
• Sarro L, Agosta F, Canu E, Riva N, Prelle A, Copetti M, et al. Cognitive functions and white matter tract damage in amyotrophic lateral sclerosis: a diffusion tensor tractography study. AJNR Am J Neuroradiol. 2011;32:1866–72.
   PubMed Web of Science ®Google Scholar
• Palmieri A, Naccarato M, Abrahams S, Bonato M, D’Ascenzo C, Balestreri S, et al. Right hemisphere dysfunction and emotional processing in ALS: an fMRI study. J Neurol. 2010;257:1970–8.
   PubMed Web of Science ®Google Scholar
• Grossman M, Anderson C, Khan A, Avants B, Elman L, McCluskey L. Impaired action knowledge in amyotrophic lateral sclerosis. Neurology 2008;71:1396–401.
   PubMed Web of Science ®Google Scholar
• Abrahams S, Goldstein LH, Suckling J, Ng V, Simmons A, Chitnis X, et al. Frontotemporal white matter changes in amyotrophic lateral sclerosis. J Neurol. 2005;252:321–31.
   PubMed Web of Science ®Google Scholar
• Abrahams S, Goldstein LH, Simmons A, Brammer M, Williams SCR, Giampietro V, et al. Word retrieval in amyotrophic lateral sclerosis: a functional magnetic resonance imaging study. Brain. 2004;127:1507–17.
   PubMed Web of Science ®Google Scholar
• Chipika RH, Finegan E, Li Hi Shing S, McKenna MC, Christidi F, Chang KM, et al. “Switchboard” malfunction in motor neuron diseases: Selective pathology of thalamic nuclei in amyotrophic lateral sclerosis and primary lateral sclerosis. Neuroimage Clin. 2020;27:102300.
   PubMed Web of Science ®Google Scholar
• Burger A, Kotze MJ, Stein DJ, Janse van Rensburg S, Howells FM. The relationship between measurement of in vivo brain glutamate and markers of iron metabolism: a proton magnetic resonance spectroscopy study in healthy adults. Eur J Neurosci. 2020;51:984–90.
   PubMed Web of Science ®Google Scholar
• Rau A, Jost WH, Demerath T, Kellner E, Reisert M, Urbach H. Diffusion microstructure imaging in progressive supranuclear palsy: reduced axonal volumes in the superior cerebellar peduncles, dentato-rubro-thalamic tracts, ventromedial thalami, and frontomesial white matter. Cereb Cortex. 2022;32:5628–36.
   PubMed Web of Science ®Google Scholar
• Würtemberger U, Rau A, Reisert M, Kellner E, Diebold M, Erny D, et al. Differentiation of perilesional edema in glioblastomas and brain metastases: comparison of diffusion tensor imaging, neurite orientation dispersion and density imaging and diffusion microstructure imaging. Cancers. 2022;15:
   PubMed Web of Science ®Google Scholar
• Jin D, Su X, Jin Y, Gu Y, Yang J, Wang Q, et al. Diagnostic value of MRI perfusion-weighted imaging and diffusion-weighted imaging parameters in cerebral apoplexy. Am J Transl Res. 2023;15:1097–106.
   PubMed Web of Science ®Google Scholar
• Suk TR, Rousseaux MWC. The role of TDP-43 mislocalization in amyotrophic lateral sclerosis. Mol Neurodegener. 2020;15:45.
   PubMed Web of Science ®Google Scholar
• Scotter EL, Chen HJ, Shaw CE. TDP-43 proteinopathy and ALS: insights into disease mechanisms and therapeutic targets. Neurotherapeutics. 2015;12:352–63.
   PubMed Web of Science ®Google Scholar
• Mackenzie IRA, Rademakers R. The role of TDP-43 in amyotrophic lateral sclerosis and frontotemporal dementia. Curr Opin Neurol. 2008;21:693–700.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Ludolph AC, Brettschneider J. TDP-43 in amyotrophic lateral sclerosis – is it a prion disease? Eur J Neurol. 2015;22:753–61.
   PubMed Web of Science ®Google Scholar
• Brettschneider J, Arai K, Del Tredici K, Toledo JB, Robinson JL, Lee EB, et al. TDP-43 pathology and neuronal loss in amyotrophic lateral sclerosis spinal cord. Acta Neuropathol. 2014;128:423–37.
   PubMed Web of Science ®Google Scholar
• Brettschneider J, Del Tredici K, Irwin DJ, Grossman M, Robinson JL, Toledo JB, et al. Sequential distribution of pTDP-43 pathology in behavioral variant frontotemporal dementia (bvFTD). Acta Neuropathol. 2014;127:423–39.
   PubMed Web of Science ®Google Scholar
• Bright F, Chan G, van Hummel A, Ittner LM, Ke YD. TDP-43 and inflammation: implications for amyotrophic lateral sclerosis and frontotemporal dementia. Int J Mol Sci 2021;22:7781.
   PubMed Web of Science ®Google Scholar
• Pasquini L, Nana AL, Toller G, Brown JA, Deng J, Staffaroni A, et al. Salience network atrophy links neuron type-specific pathobiology to loss of empathy in frontotemporal dementia. Cereb Cortex. 2020;30:5387–99.
   PubMed Web of Science ®Google Scholar
• Trojsi F, Monsurrò MR, Esposito F, Tedeschi G. Widespread structural and functional connectivity changes in amyotrophic lateral sclerosis: insights from advanced neuroimaging research. Neural Plast. 2012;2012:473538.
   PubMed Web of Science ®Google Scholar
• Mazón M, Vázquez Costa JF, Ten-Esteve A, Martí-Bonmatí L. Imaging biomarkers for the diagnosis and prognosis of neurodegenerative diseases. the example of amyotrophic lateral sclerosis. Front Neurosci. 2018;12:784.
   PubMed Web of Science ®Google Scholar
• Basaia S, Agosta F, Cividini C, Trojsi F, Riva N, Spinelli EG, et al. Structural and functional brain connectome in motor neuron diseases: a multicenter MRI study. Neurology 2020;95:e2552–e2564.
   PubMed Web of Science ®Google Scholar