{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,17]],"date-time":"2026-07-17T15:31:56Z","timestamp":1784302316636,"version":"3.55.0"},"reference-count":48,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,9,19]],"date-time":"2024-09-19T00:00:00Z","timestamp":1726704000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Neurol."],"abstract":"<jats:sec><jats:title>Background<\/jats:title><jats:p>This study aimed to assess whether quantitative susceptibility imaging (QSM)-based measures of iron accumulation in the cerebellum predict cognitive and behavioral features in non-demented amyotrophic lateral sclerosis (ALS) patients.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>A total of ALS patients underwent 3-T MRI and a clinical assessment using the ALS Functional Rating Scale-Revised (ALSFRS-R) and the Edinburgh Cognitive and Behavioural ALS Screen (ECAS). Regression models were applied to each subscale of the cognitive section of the ECAS and the ECAS-Carer Interview to examine the effect of QSM-based measures in white and gray matter (WM; GM) of the cerebellum, separately for right, left, and bilateral cerebellar regions of interest (ROIs). These effects were compared to those of cerebellar volumetrics in WM\/GM, right and left hemispheres while controlling for demographics, disease status, and total intracranial volume.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Higher QSM measures of the cerebellar GM on the left, right, and bilateral sides significantly predicted (<jats:italic>p<\/jats:italic>s\u2009\u2264\u20090.003) a greater number of errors on the executive functioning (EF) subscale of the ECAS (ECAS-EF). Moreover, higher GM-related, QSM measures of the cerebellum were associated with an increased probability of a below-cut-off performance on the ECAS-EF (<jats:italic>p<\/jats:italic>s\u2009\u2264\u20090.024). No significant effects were observed for QSM measures of the cerebellar WM or for volumetric measures on the ECAS-EF. Other ECAS measures showed no significant effects. Bilateral QSM measures of the cerebellar GM also selectively predicted performance on backward digit span and social cognition tasks.<\/jats:p><\/jats:sec><jats:sec><jats:title>Discussion<\/jats:title><jats:p>Iron accumulation within the cerebellar GM, particularly in the cerebellar cortices, may be associated with executive functioning deficits in non-demented ALS patients. Therefore, QSM-based measures could be useful for identifying the neural correlates of extra-motor cognitive deficits in ALS patients.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fneur.2024.1426841","type":"journal-article","created":{"date-parts":[[2024,9,19]],"date-time":"2024-09-19T14:26:41Z","timestamp":1726756001000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":1,"title":["QSM-detected iron accumulation in the cerebellar gray matter is selectively associated with executive dysfunction in non-demented ALS patients"],"prefix":"10.3389","volume":"15","author":[{"given":"Edoardo Nicol\u00f2","family":"Aiello","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Valeria Elisa","family":"Contarino","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giorgio","family":"Conte","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Federica","family":"Solca","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Beatrice","family":"Curti","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alessio","family":"Maranzano","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Silvia","family":"Torre","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Silvia","family":"Casale","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alberto","family":"Doretti","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eleonora","family":"Colombo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Federico","family":"Verde","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vincenzo","family":"Silani","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunlei","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Claudia","family":"Cinnante","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fabio Maria","family":"Triulzi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Claudia","family":"Morelli","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Barbara","family":"Poletti","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nicola","family":"Ticozzi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2024,9,19]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"661","DOI":"10.1038\/nrneurol.2014.184","article-title":"The phenotypic variability of amyotrophic lateral sclerosis","volume":"10","author":"Swinnen","year":"2014","journal-title":"Nat Rev Neurol"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"2335","DOI":"10.4103\/1673-5374.336139","article-title":"Cerebellar pathology in motor neuron disease: neuroplasticity and neurodegeneration","volume":"17","author":"Chipika","year":"2022","journal-title":"Neural Regen Res"},{"key":"ref3","doi-asserted-by":"publisher","first-page":"3464","DOI":"10.1002\/hbm.24609","article-title":"Precentral degeneration and cerebellar compensation in amyotrophic lateral sclerosis: a multimodal MRI analysis","volume":"40","author":"Qiu","year":"2019","journal-title":"Hum Brain Mapp"},{"key":"ref4","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1111\/ene.14042","article-title":"Adaptive functional reorganization in amyotrophic lateral sclerosis: coexisting degenerative and compensatory changes","volume":"27","author":"Abidi","year":"2020","journal-title":"Eur J Neurol"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"101389","DOI":"10.1016\/j.arr.2021.101389","article-title":"Novel insights into the relationship between cerebellum and dementia: a narrative review as a toolkit for clinicians","volume":"70","author":"Devita","year":"2021","journal-title":"Ageing Res Rev"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"e105632","DOI":"10.1371\/journal.pone.0105632","article-title":"Cerebellar integrity in the amyotrophic lateral sclerosis-frontotemporal dementia continuum","volume":"9","author":"Tan","year":"2014","journal-title":"PLoS One"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"2050","DOI":"10.1007\/s00259-016-3434-1","article-title":"Amyloid-and FDG-PET imaging in amyotrophic lateral sclerosis","volume":"43","author":"Mat\u00edas-Guiu","year":"2016","journal-title":"Eur J Nucl Med Mol Imaging"},{"key":"ref8","doi-asserted-by":"publisher","first-page":"440","DOI":"10.3389\/fnins.2019.00440","article-title":"Cognitive syndromes and C9orf72 mutation are not related to cerebellar degeneration in amyotrophic lateral sclerosis","volume":"13","author":"Consonni","year":"2019","journal-title":"Front Neurosci"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"620","DOI":"10.1212\/WNL.0000000000000693","article-title":"Impaired corticopontocerebellar tracts underlie pseudobulbar affect in motor neuron disorders","volume":"83","author":"Floeter","year":"2014","journal-title":"Neurology"},{"key":"ref10","doi-asserted-by":"publisher","first-page":"745","DOI":"10.1111\/ene.14637","article-title":"Brain metabolic correlates of apathy in amyotrophic lateral sclerosis: an 18F-FDG-positron emission tomography stud","volume":"28","author":"Canosa","year":"2021","journal-title":"Eur J Neurol"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"102385","DOI":"10.1016\/j.nicl.2020.102385","article-title":"Involvement of the dentate nucleus in the pathophysiology of amyotrophic lateral sclerosis: a multi-center and multimodal neuroimaging study","volume":"28","author":"Bharti","year":"2020","journal-title":"NeuroImage Clin"},{"key":"ref12","doi-asserted-by":"publisher","first-page":"82","DOI":"10.1002\/mrm.25358","article-title":"Quantitative susceptibility mapping (QSM): decoding MRI data for a tissue magnetic biomarker","volume":"73","author":"Wang","year":"2015","journal-title":"Magn Reson Med"},{"key":"ref13","doi-asserted-by":"publisher","first-page":"108815","DOI":"10.1016\/j.ejrad.2020.108815","article-title":"Toward a marker of upper motor neuron impairment in amyotrophic lateral sclerosis: a fully automatic investigation of the magnetic susceptibility in the precentral cortex","volume":"124","author":"Contarino","year":"2020","journal-title":"Eur J Radiol"},{"key":"ref14","doi-asserted-by":"publisher","first-page":"5272","DOI":"10.1007\/s00330-020-07547-5","article-title":"Amyotrophic lateral sclerosis phenotypes significantly differ in terms of magnetic susceptibility properties of the precentral cortex","volume":"31","author":"Conte","year":"2021","journal-title":"Eur Radiol"},{"key":"ref15","doi-asserted-by":"publisher","first-page":"942","DOI":"10.3390\/brainsci12070942","article-title":"Distribution indices of magnetic susceptibility values in the primary motor cortex enable classifying patients with amyotrophic lateral sclerosis","volume":"12","author":"Costagli","year":"2022","journal-title":"Brain Sci"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"1283","DOI":"10.1002\/jmri.27530","article-title":"Magnetic resonance iron imaging in amyotrophic lateral sclerosis","volume":"55","author":"Bhattarai","year":"2022","journal-title":"J Magn Reson Imaging"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"618435","DOI":"10.3389\/fnins.2021.618435","article-title":"Systematic review: quantitative susceptibility mapping (QSM) of brain iron profile in neurodegenerative diseases","volume":"15","author":"Ravanfar","year":"2021","journal-title":"Front Neurosci"},{"key":"ref18","author":"Verma","year":"2022"},{"key":"ref19","doi-asserted-by":"publisher","first-page":"180","DOI":"10.3389\/fnins.2019.00180","article-title":"Iron in neurodegeneration, cause or consequence?","volume":"13","author":"Ndayisaba","year":"2019","journal-title":"Front Neurosci"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"2812","DOI":"10.1007\/s12035-020-02277-7","article-title":"New insights into the role of ferritin in iron homeostasis and neurodegenerative diseases","volume":"58","author":"Zhang","year":"2021","journal-title":"Mol Neurobiol"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s13244-022-01207-6","article-title":"Brain pathological changes during neurodegenerative diseases and their identification methods: how does QSM perform in detecting this process?","volume":"13","author":"Nikparast","year":"2022","journal-title":"Insights Imaging"},{"key":"ref22","doi-asserted-by":"publisher","first-page":"293","DOI":"10.1080\/146608200300079536","article-title":"El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis","volume":"1","author":"Brooks","year":"2000","journal-title":"Amyotroph Lateral Scler Other Motor Neuron Disord"},{"key":"ref23","doi-asserted-by":"publisher","first-page":"489","DOI":"10.1080\/21678421.2016.1183679","article-title":"The validation of the Italian Edinburgh cognitive and behavioural ALS screen (ECAS)","volume":"17","author":"Poletti","year":"2016","journal-title":"Amyot Lateral Sclerosis Frontot Degen"},{"key":"ref24","doi-asserted-by":"publisher","first-page":"1006","DOI":"10.1212\/WNL.0b013e31821103e6","article-title":"Classification of primary progressive aphasia and its variants","volume":"76","author":"Gorno-Tempini","year":"2011","journal-title":"Neurology"},{"key":"ref25","doi-asserted-by":"publisher","first-page":"2456","DOI":"10.1093\/brain\/awr179","article-title":"Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia","volume":"134","author":"Rascovsky","year":"2011","journal-title":"Brain"},{"key":"ref26","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1016\/S0022-510X(99)00210-5","article-title":"The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function","volume":"169","author":"Cedarbaum","year":"1999","journal-title":"J Neurol Sci"},{"key":"ref27","doi-asserted-by":"publisher","first-page":"941","DOI":"10.1007\/s10072-022-06505-x","article-title":"Diagnostic properties of the Italian ECAS Carer interview (ECAS-CI)","volume":"44","author":"Poletti","year":"2023","journal-title":"Neurol Sci"},{"key":"ref28","doi-asserted-by":"publisher","first-page":"774","DOI":"10.1016\/j.neuroimage.2012.01.021","article-title":"Free surfer","volume":"62","author":"Fischl","year":"2012","journal-title":"NeuroImage"},{"key":"ref29","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1002\/jmri.24768","article-title":"Susceptibility-weighted imaging and quantitative susceptibility mapping in the brain","volume":"42","author":"Liu","year":"2015","journal-title":"J Magn Reson Imaging"},{"key":"ref30","doi-asserted-by":"publisher","first-page":"143","DOI":"10.1002\/hbm.10062","article-title":"Fast robust automated brain extraction","volume":"17","author":"Smith","year":"2002","journal-title":"Hum Brain Mapp"},{"key":"ref31","doi-asserted-by":"publisher","first-page":"1294","DOI":"10.1002\/nbm.3383","article-title":"Streaking artifact reduction for quantitative susceptibility mapping of sources with large dynamic range","volume":"28","author":"Wei","year":"2015","journal-title":"NMR Biomed"},{"key":"ref32","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1016\/j.neuroimage.2014.12.043","article-title":"A method for estimating and removing streaking artifacts in quantitative susceptibility mapping","volume":"108","author":"Li","year":"2015","journal-title":"NeuroImage"},{"key":"ref33","doi-asserted-by":"publisher","first-page":"52","DOI":"10.5395\/rde.2013.38.1.52","article-title":"Statistical notes for clinical researchers: assessing normal distribution (2) using skewness and kurtosis","volume":"38","author":"Kim","year":"2013","journal-title":"Restorative Dent Endod"},{"key":"ref34","doi-asserted-by":"publisher","first-page":"2766","DOI":"10.1890\/07-0043.1","article-title":"Quasi-Poisson vs. negative binomial regression: how should we model overdispersed count data?","volume":"88","author":"Ver Hoef","year":"2007","journal-title":"Ecology"},{"key":"ref35","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1080\/21678421.2021.1946085","article-title":"Italian adaptation of the Beaumont behavioral inventory (BBI): psychometric properties and clinical usability","volume":"23","author":"Iazzolino","year":"2022","journal-title":"Amyot Lateral Sclerosis Frontot Degen"},{"key":"ref36","doi-asserted-by":"publisher","first-page":"5397","DOI":"10.1007\/s10072-022-06157-x","article-title":"Cognition and motor phenotypes in ALS: a retrospective study","volume":"43","author":"Aiello","year":"2022","journal-title":"Neurol Sci"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"S273","DOI":"10.1007\/s10072-020-04753-3","article-title":"Usability of the negative binomial model for analyzing ceiling and highly-inter-individually-variable cognitive data","volume":"41","author":"Aiello","year":"2020","journal-title":"Neurol Sci"},{"key":"ref38","doi-asserted-by":"publisher","first-page":"393","DOI":"10.3390\/biomedicines12020393","article-title":"Modelling the distribution of cognitive outcomes for early-stage neurocognitive disorders: a model comparison approach","volume":"12","author":"Saffari","year":"2024","journal-title":"Biomedicine"},{"key":"ref39","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1080\/09720502.2010.10700699","article-title":"Collinearity diagnostics of binary logistic regression model","volume":"13","author":"Midi","year":"2010","journal-title":"J Interdis Math"},{"key":"ref40","doi-asserted-by":"publisher","first-page":"422","DOI":"10.1007\/s11065-020-09465-1","article-title":"Cerebellar-subcortical-cortical systems as modulators of cognitive functions","volume":"31","author":"Clark","year":"2021","journal-title":"Neuropsychol Rev"},{"key":"ref41","doi-asserted-by":"publisher","first-page":"184","DOI":"10.1080\/14734220601169707","article-title":"Cerebellar involvement in executive control","volume":"6","author":"Bellebaum","year":"2007","journal-title":"Cerebellum"},{"key":"ref42","doi-asserted-by":"publisher","first-page":"1781","DOI":"10.1016\/j.neuropsychologia.2004.04.023","article-title":"Shared and distinct neurophysiological components of the digits forward and backward tasks as revealed by functional neuroimaging","volume":"42","author":"Gerton","year":"2004","journal-title":"Neuropsychologia"},{"key":"ref43","doi-asserted-by":"publisher","first-page":"180","DOI":"10.3389\/fnhum.2019.00180","article-title":"Neural correlates of verbal working memory: an fMRI meta-analysis","volume":"13","author":"Emch","year":"2019","journal-title":"Front Hum Neurosci"},{"key":"ref44","doi-asserted-by":"publisher","first-page":"306","DOI":"10.1093\/brain\/awh685","article-title":"Cerebellar damage produces selective deficits in verbal working memory","volume":"129","author":"Ravizza","year":"2006","journal-title":"Brain"},{"key":"ref45","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1016\/j.neuropsychologia.2011.11.017","article-title":"Distinct critical cerebellar subregions for components of verbal working memory","volume":"50","author":"Cooper","year":"2012","journal-title":"Neuropsychologia"},{"key":"ref46","doi-asserted-by":"publisher","first-page":"833","DOI":"10.1007\/s12311-020-01155-1","article-title":"Consensus paper: cerebellum and social cognition","volume":"19","author":"Van Overwalle","year":"2020","journal-title":"Cerebellum"},{"key":"ref47","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1080\/21678421.2016.1267768","article-title":"Amyotrophic lateral sclerosis-frontotemporal spectrum disorder (ALS-FTSD): revised diagnostic criteria","volume":"18","author":"Strong","year":"2017","journal-title":"Amyot Lateral Sclerosis Frontot Degen"},{"key":"ref48","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1016\/j.neuroimage.2009.01.045","article-title":"A probabilistic MR atlas of the human cerebellum","volume":"46","author":"Diedrichsen","year":"2009","journal-title":"NeuroImage"}],"container-title":["Frontiers in Neurology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fneur.2024.1426841\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,9,19]],"date-time":"2024-09-19T14:26:43Z","timestamp":1726756003000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fneur.2024.1426841\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,9,19]]},"references-count":48,"alternative-id":["10.3389\/fneur.2024.1426841"],"URL":"https:\/\/doi.org\/10.3389\/fneur.2024.1426841","relation":{},"ISSN":["1664-2295"],"issn-type":[{"value":"1664-2295","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,9,19]]},"article-number":"1426841"}}