Supra- and infra-tentorial degeneration patterns in primary lateral sclerosis: a multimodal longitudinal neuroradiology study.
Cerebellum
Connectivity
MRI
Pharmaceutical trials
Primary Lateral Sclerosis
Journal
Journal of neurology
ISSN: 1432-1459
Titre abrégé: J Neurol
Pays: Germany
ID NLM: 0423161
Informations de publication
Date de publication:
05 Mar 2024
05 Mar 2024
Historique:
received:
21
12
2023
accepted:
15
02
2024
revised:
14
02
2024
medline:
5
3
2024
pubmed:
5
3
2024
entrez:
4
3
2024
Statut:
aheadofprint
Résumé
Primary lateral sclerosis (PLS) is traditionally solely associated with progressive upper motor neuron dysfunction manifesting in limb spasticity, gait impairment, bulbar symptoms and pseudobulbar affect. Recent studies have described frontotemporal dysfunction in some patients resulting in cognitive manifestations. Cerebellar pathology is much less well characterised despite sporadic reports of cerebellar disease. A multi-timepoint, longitudinal neuroimaging study was conducted to characterise the evolution of both intra-cerebellar disease burden and cerebro-cerebellar connectivity. The volumes of deep cerebellar nuclei, cerebellar cortical volumes, cerebro-cerebellar structural and functional connectivity were assessed longitudinally in a cohort of 43 individuals with PLS. Cerebello-frontal, -temporal, -parietal, -occipital and cerebello-thalamic structural disconnection was detected at baseline based on radial diffusivity (RD) and cerebello-frontal decoupling was also evident based on fractional anisotropy (FA) alterations. Functional connectivity changes were also detected in cerebello-frontal, parietal and occipital projections. Volume reductions were identified in the vermis, anterior lobe, posterior lobe, and crura. Among the deep cerebellar nuclei, the dorsal dentate was atrophic. Longitudinal follow-up did not capture statistically significant progressive changes. Significant primary motor cortex atrophy and inter-hemispheric transcallosal degeneration were also captured. PLS is not only associated with upper motor neuron dysfunction, but cerebellar cortical volume loss and deep cerebellar nuclear atrophy can also be readily detected. In addition to intra-cerebellar disease burden, cerebro-cerebellar connectivity alterations also take place. Our data add to the evolving evidence of widespread neurodegeneration in PLS beyond the primary motor regions. Cerebellar dysfunction in PLS is likely to exacerbate bulbar, gait and dexterity impairment and contribute to pseudobulbar affect.
Sections du résumé
BACKGROUND
BACKGROUND
Primary lateral sclerosis (PLS) is traditionally solely associated with progressive upper motor neuron dysfunction manifesting in limb spasticity, gait impairment, bulbar symptoms and pseudobulbar affect. Recent studies have described frontotemporal dysfunction in some patients resulting in cognitive manifestations. Cerebellar pathology is much less well characterised despite sporadic reports of cerebellar disease.
METHODS
METHODS
A multi-timepoint, longitudinal neuroimaging study was conducted to characterise the evolution of both intra-cerebellar disease burden and cerebro-cerebellar connectivity. The volumes of deep cerebellar nuclei, cerebellar cortical volumes, cerebro-cerebellar structural and functional connectivity were assessed longitudinally in a cohort of 43 individuals with PLS.
RESULTS
RESULTS
Cerebello-frontal, -temporal, -parietal, -occipital and cerebello-thalamic structural disconnection was detected at baseline based on radial diffusivity (RD) and cerebello-frontal decoupling was also evident based on fractional anisotropy (FA) alterations. Functional connectivity changes were also detected in cerebello-frontal, parietal and occipital projections. Volume reductions were identified in the vermis, anterior lobe, posterior lobe, and crura. Among the deep cerebellar nuclei, the dorsal dentate was atrophic. Longitudinal follow-up did not capture statistically significant progressive changes. Significant primary motor cortex atrophy and inter-hemispheric transcallosal degeneration were also captured.
CONCLUSIONS
CONCLUSIONS
PLS is not only associated with upper motor neuron dysfunction, but cerebellar cortical volume loss and deep cerebellar nuclear atrophy can also be readily detected. In addition to intra-cerebellar disease burden, cerebro-cerebellar connectivity alterations also take place. Our data add to the evolving evidence of widespread neurodegeneration in PLS beyond the primary motor regions. Cerebellar dysfunction in PLS is likely to exacerbate bulbar, gait and dexterity impairment and contribute to pseudobulbar affect.
Identifiants
pubmed: 38438819
doi: 10.1007/s00415-024-12261-z
pii: 10.1007/s00415-024-12261-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Health Research Board
ID : JPND-Cofund-2-2019-1
Pays : Ireland
Organisme : Health Research Board
ID : HRB EIA-2017-019
Pays : Ireland
Informations de copyright
© 2024. The Author(s).
Références
Carew JD, Nair G, Pineda-Alonso N, Usher S, Hu X, Benatar M (2011) Magnetic resonance spectroscopy of the cervical cord in amyotrophic lateral sclerosis. Amyotrophic Lateral Scler 12(3):185–191. https://doi.org/10.3109/17482968.2010.515223
doi: 10.3109/17482968.2010.515223
Ta D, Ishaque AH, Elamy A, Anand T, Wu A, Eurich DT, Luk C, Yang YH, Kalra S (2023) Severity of in vivo corticospinal tract degeneration is associated with survival in amyotrophic lateral sclerosis: a longitudinal, multicohort study. Eur J Neurol. https://doi.org/10.1111/ene.15686
doi: 10.1111/ene.15686
Ferraro PM, Agosta F, Riva N, Copetti M, Spinelli EG, Falzone Y, Sorarù G, Comi G, Chiò A, Filippi M (2017) Multimodal structural MRI in the diagnosis of motor neuron diseases. NeuroImage Clinical 16:240–247. https://doi.org/10.1016/j.nicl.2017.08.002
doi: 10.1016/j.nicl.2017.08.002
pmcid: 5545829
Pioro EP, Turner MR, Bede P (2020) Neuroimaging in primary lateral sclerosis. Amyotrophic Lateral Scler Frontotemporal Degener 21(sup1):18–27. https://doi.org/10.1080/21678421.2020.1837176
doi: 10.1080/21678421.2020.1837176
Clark MG, Smallwood Shoukry R, Huang CJ, Danielian LE, Bageac D, Floeter MK (2018) Loss of functional connectivity is an early imaging marker in primary lateral sclerosis. Amyotrophic Lateral Scler Frontotemporal Degener. https://doi.org/10.1080/21678421.2018.1517180
doi: 10.1080/21678421.2018.1517180
Floeter MK, Mills R (2009) Progression in primary lateral sclerosis: a prospective analysis. Amyotroph Lateral Scler 10(5–6):339–346
doi: 10.3109/17482960903171136
pmcid: 3434688
Tahedl M, Li Hi Shing S, Finegan E, Chipika RH, Lope J, Hardiman O, Bede P (2021) Propagation patterns in motor neuron diseases: individual and phenotype-associated disease-burden trajectories across the UMN-LMN spectrum of MNDs. Neurobiol Aging 109:78–87. https://doi.org/10.1016/j.neurobiolaging.2021.04.031
doi: 10.1016/j.neurobiolaging.2021.04.031
de Vries BS, Rustemeijer LMM, Bakker LA, Schröder CD, Veldink JH, van den Berg LH, Nijboer TCW, van Es MA (2019) Cognitive and behavioural changes in PLS and PMA:challenging the concept of restricted phenotypes. J Neurol Neurosurg Psychiatry 90(2):141–147. https://doi.org/10.1136/jnnp-2018-318788
doi: 10.1136/jnnp-2018-318788
Finegan E, Shing SLH, Chipika RH, Chang KM, McKenna MC, Doherty MA, Hengeveld JC, Vajda A, Pender N, Donaghy C, Hutchinson S, McLaughlin RL, Hardiman O, Bede P (2021) Extra-motor cerebral changes and manifestations in primary lateral sclerosis. Brain Imaging Behav. https://doi.org/10.1007/s11682-020-00421-4
doi: 10.1007/s11682-020-00421-4
Le Forestier N, Maisonobe T, Piquard A, Rivaud S, Crevier-Buchman L, Salachas F, Pradat PF, Lacomblez L, Meininger V (2001) Does primary lateral sclerosis exist? A study of 20 patients and a review of the literature. Brain: J Neurol 124(Pt 10):1989–1999
doi: 10.1093/brain/124.10.1989
Bede P, Pradat PF, Lope J, Vourc’h P, Blasco H, Corcia P (2021) Primary lateral sclerosis: clinical, radiological and molecular features. Rev Neurol. https://doi.org/10.1016/j.neurol.2021.04.008
doi: 10.1016/j.neurol.2021.04.008
de Vries BS, Spreij LA, Rustemeijer LMM, Bakker LA, Veldink JH, van den Berg LH, Nijboer TCW, van Es MA (2019) A neuropsychological and behavioral study of PLS. Amyotrophic Lateral Scler Frontotemporal Degener 20(5–6):376–384. https://doi.org/10.1080/21678421.2019.1620284
doi: 10.1080/21678421.2019.1620284
Finegan E, Li Hi Shing S, Chipika RH, Doherty MA, Hengeveld JC, Vajda A, Donaghy C, Pender N, McLaughlin RL, Hardiman O, Bede P (2019) Widespread subcortical grey matter degeneration in primary lateral sclerosis: a multimodal imaging study with genetic profiling. NeuroImage Clin 24:102089. https://doi.org/10.1016/j.nicl.2019.102089
doi: 10.1016/j.nicl.2019.102089
pmcid: 6978214
Chipika RH, Christidi F, Finegan E, Li Hi Shing S, McKenna MC, Chang KM, Karavasilis E, Doherty MA, Hengeveld JC, Vajda A, Pender N, Hutchinson S, Donaghy C, McLaughlin RL, Hardiman O, Bede P (2020) Amygdala pathology in amyotrophic lateral sclerosis and primary lateral sclerosis. J Neurol Sci 417:117039. https://doi.org/10.1016/j.jns.2020.117039
doi: 10.1016/j.jns.2020.117039
Chipika RH, Finegan E, Li Hi Shing S, McKenna MC, Christidi F, Chang KM, Doherty MA, Hengeveld JC, Vajda A, Pender N, Hutchinson S, Donaghy C, McLaughlin RL, Hardiman O, Bede P (2020) “Switchboard” malfunction in motor neuron diseases: selective pathology of thalamic nuclei in amyotrophic lateral sclerosis and primary lateral sclerosis. NeuroImage Clin 27:102300. https://doi.org/10.1016/j.nicl.2020.102300
doi: 10.1016/j.nicl.2020.102300
pmcid: 7303672
Hubers A, Kassubek J, Gron G, Gorges M, Aho-Oezhan H, Keller J, Horn H, Neugebauer H, Uttner I, Lule D, Ludolph AC (2016) Pathological laughing and crying in amyotrophic lateral sclerosis is related to frontal cortex function. J Neurol 263(9):1788–1795. https://doi.org/10.1007/s00415-016-8201-5
doi: 10.1007/s00415-016-8201-5
Bede P, Finegan E (2018) Revisiting the pathoanatomy of pseudobulbar affect: mechanisms beyond corticobulbar dysfunction. Amyotrophic Lateral Scler Frontotemporal Degener 19(1–2):4–6. https://doi.org/10.1080/21678421.2017.1392578
doi: 10.1080/21678421.2017.1392578
Parvizi J, Anderson SW, Martin CO, Damasio H, Damasio AR (2001) Pathological laughter and crying: a link to the cerebellum. Brain: J Neurol 124(Pt 9):1708–1719
doi: 10.1093/brain/124.9.1708
Floeter MK, Katipally R, Kim MP, Schanz O, Stephen M, Danielian L, Wu T, Huey ED, Meoded A (2014) Impaired corticopontocerebellar tracts underlie pseudobulbar affect in motor neuron disorders. Neurology 83(7):620–627. https://doi.org/10.1212/wnl.0000000000000693
doi: 10.1212/wnl.0000000000000693
pmcid: 4141995
Finegan E, Chipika RH, Li Hi Shing S, Hardiman O, Bede P (2019) Pathological crying and laughing in motor neuron disease: pathobiology, screening. Intervention Front Neurol 10:260. https://doi.org/10.3389/fneur.2019.00260
doi: 10.3389/fneur.2019.00260
Argyropoulos GD, Christidi F, Karavasilis E, Velonakis G, Antoniou A, Bede P, Seimenis I, Kelekis N, Douzenis A, Papakonstantinou O, Efstathopoulos E, Ferentinos P (2021) Cerebro-cerebellar white matter connectivity in bipolar disorder and associated polarity subphenotypes. Prog Neuropsychopharmacol Biol Psychiatry 104:110034. https://doi.org/10.1016/j.pnpbp.2020.110034
doi: 10.1016/j.pnpbp.2020.110034
Christidi F, Karavasilis E, Ferentinos P, Xirou S, Velonakis G, Rentzos M, Zouvelou V, Zalonis I, Efstathopoulos E, Kelekis N, Evdokimidis I (2017) Investigating the neuroanatomical substrate of pathological laughing and crying in amyotrophic lateral sclerosis with multimodal neuroimaging techniques. Amyotrophic Lateral Scler Frontotemporal Degener. https://doi.org/10.1080/21678421.2017.1386689
doi: 10.1080/21678421.2017.1386689
Trojsi F, Di Nardo F, D’Alvano G, Caiazzo G, Passaniti C, Mangione A, Sharbafshaaer M, Russo A, Silvestro M, Siciliano M, Cirillo M, Tedeschi G, Esposito F (2023) Resting state fMRI analysis of pseudobulbar affect in amyotrophic lateral sclerosis (ALS): motor dysfunction of emotional expression. Brain Imaging Behav 17(1):77–89. https://doi.org/10.1007/s11682-022-00744-4
doi: 10.1007/s11682-022-00744-4
Finegan E, Chipika RH, Doherty MA, McLaughlin RL, Iyer PM, Donaghy C, Hardiman O, Bede P (2018) Primary lateral sclerosis, part of the MND spectrum or distinct entity: a multiparametric neuroimaging study with comprehensive clinical and genetic profiling. Amyotrophic Lateral Scler Frontotemporal Degener 19:11–12. https://doi.org/10.1080/21678421.2018.1510202
doi: 10.1080/21678421.2018.1510202
Tahedl M, Tan EL, Shing SLH, Chipika RH, Siah WF, Hengeveld JC, Doherty MA, McLaughlin RL, Hardiman O, Finegan E, Bede P (2023) Not a benign motor neuron disease: longitudinal imaging captures relentless motor connectome disintegration in primary lateral sclerosis. Eur J Neurol 30(5):1232–1245. https://doi.org/10.1111/ene.15725
doi: 10.1111/ene.15725
Mackenzie IRA, Briemberg H (2020) TDP-43 pathology in primary lateral sclerosis. Amyotrophic Lateral Scler Frontotemporal Degener 21(sup1):52–58. https://doi.org/10.1080/21678421.2020.1790607
doi: 10.1080/21678421.2020.1790607
Turner MR, Barohn RJ, Corcia P, Fink JK, Harms MB, Kiernan MC, Ravits J, Silani V, Simmons Z, Statland J, van den Berg LH, Mitsumoto H (2020) Primary lateral sclerosis: consensus diagnostic criteria. J Neurol Neurosurg Psychiatry 91(4):373–377. https://doi.org/10.1136/jnnp-2019-322541
doi: 10.1136/jnnp-2019-322541
Finegan E, Siah WF, Shing SLH, Chipika RH, Chang KM, McKenna MC, Doherty MA, Hengeveld JC, Vajda A, Donaghy C, Hutchinson S, McLaughlin RL, Hardiman O, Bede P (2020) Imaging and clinical data indicate considerable disease burden in ‘probable’ PLS: patients with UMN symptoms for 2–4 years. Data Brief. https://doi.org/10.1016/j.dib.2020.106247
doi: 10.1016/j.dib.2020.106247
pmcid: 7481824
Tan CF, Kakita A, Piao YS, Kikugawa K, Endo K, Tanaka M, Okamoto K, Takahashi H (2003) 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 Neuropathol 105(6):615–620
doi: 10.1007/s00401-003-0687-0
Canu E, Agosta F, Galantucci S, Chio A, Riva N, Silani V, Falini A, Comi G, Filippi M (2013) Extramotor damage is associated with cognition in primary lateral sclerosis patients. PLoS ONE [Electronic Resource] 8(12):e82017
doi: 10.1371/journal.pone.0082017
Finegan E, Chipika RH, Li Hi Shing S, Doherty MA, Hengeveld JC, Vajda A, Donaghy C, McLaughlin RL, Pender N, Hardiman O, Bede P (2019) The clinical and radiological profile of primary lateral sclerosis: a population-based study. J Neurol 266(11):2718–2733. https://doi.org/10.1007/s00415-019-09473-z
doi: 10.1007/s00415-019-09473-z
Finegan E, Siah WF, Li Hi Shing S, Chipika RH, Hardiman O, Bede P (2022) Cerebellar degeneration in primary lateral sclerosis: an under-recognized facet of PLS. Amyotrophic Lateral Scler Frontotemporal Degener. https://doi.org/10.1080/21678421.2021.2023188
doi: 10.1080/21678421.2021.2023188
Agosta F, Galantucci S, Riva N, Chio A, Messina S, Iannaccone S, Calvo A, Silani V, Copetti M, Falini A, Comi G, Filippi M (2014) Intrahemispheric and interhemispheric structural network abnormalities in PLS and ALS. Hum Brain Mapp 35(4):1710–1722
doi: 10.1002/hbm.22286
Meoded A, Morrissette AE, Katipally R, Schanz O, Gotts SJ, Floeter MK (2015) Cerebro-cerebellar connectivity is increased in primary lateral sclerosis. NeuroImage Clinical 7:288–296
doi: 10.1016/j.nicl.2014.12.009
Tu S, Menke RAL, Talbot K, Kiernan MC, Turner MR (2019) Cerebellar tract alterations in PLS and ALS. Amyotrophic Lateral Scler Frontotemporal Degener 20(3–4):281–284. https://doi.org/10.1080/21678421.2018.1562554
doi: 10.1080/21678421.2018.1562554
Bede P, Chipika RH, Finegan E, Li Hi Shing S, Doherty MA, Hengeveld JC, Vajda A, Hutchinson S, Donaghy C, McLaughlin RL, Hardiman O (2019) Brainstem pathology in amyotrophic lateral sclerosis and primary lateral sclerosis: a longitudinal neuroimaging study. NeuroImage Clin 24:102054. https://doi.org/10.1016/j.nicl.2019.102054
doi: 10.1016/j.nicl.2019.102054
pmcid: 6849418
Bede P, Chipika RH, Finegan E, Li Hi Shing S, Chang KM, Doherty MA, Hengeveld JC, Vajda A, Hutchinson S, Donaghy C, McLaughlin RL, Hardiman O (2020) Progressive brainstem pathology in motor neuron diseases: imaging data from amyotrophic lateral sclerosis and primary lateral sclerosis. Data Brief 29:105229. https://doi.org/10.1016/j.dib.2020.105229
doi: 10.1016/j.dib.2020.105229
pmcid: 7016370
Barohn RJ, Fink JK, Heiman-Patterson T, Huey ED, Murphy J, Statland JM, Turner MR, Elman L (2020) The clinical spectrum of primary lateral sclerosis. Amyotrophic Lateral Scler Frontotemporal Degener 21(sup1):3–10. https://doi.org/10.1080/21678421.2020.1837178
doi: 10.1080/21678421.2020.1837178
Chipika RH, Mulkerrin G, Pradat PF, Murad A, Ango F, Raoul C, Bede P (2022) Cerebellar pathology in motor neuron disease: neuroplasticity and neurodegeneration. Neural Regen Res 17(11):2335–2341. https://doi.org/10.4103/1673-5374.336139
doi: 10.4103/1673-5374.336139
pmcid: 9120698
Bede P, Chipika RH, Christidi F, Hengeveld JC, Karavasilis E, Argyropoulos GD, Lope J, Li Hi Shing S, Velonakis G, Dupuis L, Doherty MA, Vajda A, McLaughlin RL, Hardiman O (2021) Genotype-associated cerebellar profiles in ALS: focal cerebellar pathology and cerebro-cerebellar connectivity alterations. J Neurol Neurosurg Psychiatry 92(11):1197–1205. https://doi.org/10.1136/jnnp-2021-326854
doi: 10.1136/jnnp-2021-326854
Floeter MK, Warden D, Lange D, Wymer J, Paganoni S, Mitsumoto H (2020) Clinical care and therapeutic trials in PLS. Amyotrophic Lateral Scler Frontotemporal Degener 21(sup1):67–73. https://doi.org/10.1080/21678421.2020.1837180
doi: 10.1080/21678421.2020.1837180
Donaghy C, Thurtell MJ, Pioro EP, Gibson JM, Leigh RJ (2011) Eye movements in amyotrophic lateral sclerosis and its mimics: a review with illustrative cases. J Neurol Neurosurg Psychiatry 82(1):110–116. https://doi.org/10.1136/jnnp.2010.212407
doi: 10.1136/jnnp.2010.212407
Proudfoot M, Menke RAL, Sharma R, Berna CM, Hicks SL, Kennard C, Talbot K, Turner MR (2015) Eye-tracking in amyotrophic lateral sclerosis: a longitudinal study of saccadic and cognitive tasks. Amyotrophic Lateral Scler Frontotemporal Degener 17(1–2):101–111. https://doi.org/10.3109/21678421.2015.1054292
doi: 10.3109/21678421.2015.1054292
Malm J, Kristensen B, Karlsson T, Carlberg B, Fagerlund M, Olsson T (1998) Cognitive impairment in young adults with infratentorial infarcts. Neurology 51(2):433–440. https://doi.org/10.1212/wnl.51.2.433
doi: 10.1212/wnl.51.2.433
Yunusova Y, Plowman EK, Green JR, Barnett C, Bede P (2019) Clinical measures of bulbar dysfunction in ALS. Front Neurol 10:106. https://doi.org/10.3389/fneur.2019.00106
doi: 10.3389/fneur.2019.00106
pmcid: 6389633
Sasegbon A, Hamdy S (2021) The role of the cerebellum in swallowing. Dysphagia. https://doi.org/10.1007/s00455-021-10271-x
doi: 10.1007/s00455-021-10271-x
pmcid: 10006062
Stoodley CJ, Schmahmann JD (2009) Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage 44(2):489–501. https://doi.org/10.1016/j.neuroimage.2008.08.039
doi: 10.1016/j.neuroimage.2008.08.039
Argyropoulos GPD, van Dun K, Adamaszek M, Leggio M, Manto M, Masciullo M, Molinari M, Stoodley CJ, Van Overwalle F, Ivry RB, Schmahmann JD (2020) The cerebellar cognitive affective/schmahmann syndrome: a task force paper. Cerebellum 19(1):102–125. https://doi.org/10.1007/s12311-019-01068-8
doi: 10.1007/s12311-019-01068-8
Christidi F, Karavasilis E, Rentzos M, Kelekis N, Evdokimidis I, Bede P (2018) Clinical and radiological markers of extra-motor deficits in amyotrophic lateral sclerosis. Front Neurol 9:1005. https://doi.org/10.3389/fneur.2018.01005
doi: 10.3389/fneur.2018.01005
pmcid: 6262087
Burke T, Pinto-Grau M, Lonergan K, Elamin M, Bede P, Costello E, Hardiman O, Pender N (2016) Measurement of social cognition in amyotrophic lateral sclerosis: a population based study. PLoS ONE 11(8):e0160850. https://doi.org/10.1371/journal.pone.0160850
doi: 10.1371/journal.pone.0160850
pmcid: 4996502
Burke T, Elamin M, Bede P, Pinto-Grau M, Lonergan K, Hardiman O, Pender N (2016) Discordant performance on the “Reading the Mind in the Eyes” Test, based on disease onset in amyotrophic lateral sclerosis. Amyotrophic Lateral Scler Frontotemporal Degener. https://doi.org/10.1080/21678421.2016.1177088
doi: 10.1080/21678421.2016.1177088
Finegan E, Shing SLH, Chipika RH, Chang KM, McKenna MC, Doherty MA, Hengeveld JC, Vajda A, Pender N, Donaghy C, Hutchinson S, McLaughlin RL, Hardiman O, Bede P (2021) Extra-motor cerebral changes and manifestations in primary lateral sclerosis. Brain Imaging Behav 15(5):2283–2296. https://doi.org/10.1007/s11682-020-00421-4
doi: 10.1007/s11682-020-00421-4
Abel O, Shatunov A, Jones AR, Andersen PM, Powell JF, Al-Chalabi A (2013) Development of a smartphone app for a genetics website: the amyotrophic lateral sclerosis online genetics database (ALSoD). JMIR Mhealth Uhealth 1(2):e18–e18. https://doi.org/10.2196/mhealth.2706
doi: 10.2196/mhealth.2706
pmcid: 4114449
Klebe S, Stevanin G, Depienne C (2015) Clinical and genetic heterogeneity in hereditary spastic paraplegias: from SPG1 to SPG72 and still counting. Rev Neurol 171(6–7):505–530. https://doi.org/10.1016/j.neurol.2015.02.017
doi: 10.1016/j.neurol.2015.02.017
Gaser C, Dahnke R, Thompson PM, Kurth F, Luders E, Initiative AsDN (2023) CAT – a computational anatomy toolbox for the analysis of structural MRI data. Biorxiv. https://doi.org/10.1101/2022.06.11.495736
doi: 10.1101/2022.06.11.495736
Diedrichsen J (2006) A spatially unbiased atlas template of the human cerebellum. Neuroimage 33(1):127–138. https://doi.org/10.1016/j.neuroimage.2006.05.056
doi: 10.1016/j.neuroimage.2006.05.056
Amunts K, Mohlberg H, Bludau S, Zilles K (2020) Julich-brain: a 3D probabilistic atlas of the human brain’s cytoarchitecture. Science 369(6506):988–992. https://doi.org/10.1126/science.abb4588
doi: 10.1126/science.abb4588
Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25(4):1325–1335. https://doi.org/10.1016/j.neuroimage.2004.12.034
doi: 10.1016/j.neuroimage.2004.12.034
Tournier J-D, Calamante F, Connelly A (2012) MRtrix: diffusion tractography in crossing fiber regions. Int J Imaging Syst Technol 22(1):53–66. https://doi.org/10.1002/ima.22005
doi: 10.1002/ima.22005
Tournier JD, Calamante F, Connelly A (2007) Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. Neuroimage 35(4):1459–1472. https://doi.org/10.1016/j.neuroimage.2007.02.016
doi: 10.1016/j.neuroimage.2007.02.016
Raffelt D, Dhollander T, Tournier JD, Tabbara R, Smith R, Pierre E, Connelly A (2017) Bias field correction and intensity normalisation for quantitative analysis of apparent fibre density. Proc ISMRM 26:3541
Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15(1):273–289. https://doi.org/10.1006/nimg.2001.0978
doi: 10.1006/nimg.2001.0978
Tournier JD, Calamante F, Connelly A (2010) Improved probabilistic streamlines tractography by 2nd order integration over fibre orientation distributions. Proceedings of the international society for magnetic resonance in medicine (ISMRM) 18
Calamante F, Tournier JD, Jackson GD, Connelly A (2010) Track-density imaging (TDI): super-resolution white matter imaging using whole-brain track-density mapping. Neuroimage 53(4):1233–1243. https://doi.org/10.1016/j.neuroimage.2010.07.024
doi: 10.1016/j.neuroimage.2010.07.024
Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM (2012) FSL. Neuroimage 62(2):782–790. https://doi.org/10.1016/j.neuroimage.2011.09.015
doi: 10.1016/j.neuroimage.2011.09.015
Pruim RHR, Mennes M, van Rooij D, Llera A, Buitelaar JK, Beckmann CF (2015) ICA-AROMA: a robust ICA-based strategy for removing motion artifacts from fMRI data. Neuroimage 112:267–277. https://doi.org/10.1016/j.neuroimage.2015.02.064
doi: 10.1016/j.neuroimage.2015.02.064
Oosterhof NN, Connolly AC, Haxby JV (2016) CoSMoMVPA: multi-modal multivariate pattern analysis of neuroimaging data in matlab/GNU octave. Front Neuroinform 10:27. https://doi.org/10.3389/fninf.2016.00027
doi: 10.3389/fninf.2016.00027
pmcid: 4956688
Tedesco AM, Chiricozzi FR, Clausi S, Lupo M, Molinari M, Leggio MG (2011) The cerebellar cognitive profile. Brain 134(12):3672–3686. https://doi.org/10.1093/brain/awr266
doi: 10.1093/brain/awr266
Van Overwalle F, D’Aes T, Marien P (2015) Social cognition and the cerebellum: a meta-analytic connectivity analysis. Hum Brain Mapp 36(12):5137–5154. https://doi.org/10.1002/hbm.23002
doi: 10.1002/hbm.23002
pmcid: 6869534
Runnqvist E, Bonnard M, Gauvin HS, Attarian S, Trébuchon A, Hartsuiker RJ, Alario FX (2016) Internal modeling of upcoming speech: a causal role of the right posterior cerebellum in non-motor aspects of language production. Cortex 81:203–214. https://doi.org/10.1016/j.cortex.2016.05.008
doi: 10.1016/j.cortex.2016.05.008
Levisohn L, Cronin-Golomb A, Schmahmann JD (2000) Neuropsychological consequences of cerebellar tumour resection in children: cerebellar cognitive affective syndrome in a paediatric population. Brain 123(5):1041–1050. https://doi.org/10.1093/brain/123.5.1041
doi: 10.1093/brain/123.5.1041
Tu S, Menke RAL, Talbot K, Kiernan MC, Turner MR (2019) Cerebellar tract alterations in PLS and ALS. Amyotroph Lateral Scler Frontotemporal Degener 20(3–4):281–284. https://doi.org/10.1080/21678421.2018.1562554
doi: 10.1080/21678421.2018.1562554
Meoded A, Morrissette AE, Katipally R, Schanz O, Gotts SJ, Floeter MK (2015) Cerebro-cerebellar connectivity is increased in primary lateral sclerosis. Neuroimage Clin 7:288–296. https://doi.org/10.1016/j.nicl.2014.12.009
doi: 10.1016/j.nicl.2014.12.009
Canu E, Agosta F, Galantucci S, Chiò A, Riva N, Silani V, Falini A, Comi G, Filippi M (2013) Extramotor damage is associated with cognition in primary lateral sclerosis patients. PLoS ONE 8(12):e82017. https://doi.org/10.1371/journal.pone.0082017
doi: 10.1371/journal.pone.0082017
pmcid: 3857796
Proudfoot M, Bede P, Turner MR (2018) Imaging cerebral activity in amyotrophic lateral sclerosis. Front Neurol 9:1148. https://doi.org/10.3389/fneur.2018.01148
doi: 10.3389/fneur.2018.01148
Abidi M, de Marco G, Grami F, Termoz N, Couillandre A, Querin G, Bede P, Pradat PF (2021) Neural correlates of motor imagery of gait in amyotrophic lateral sclerosis. J Magn Reson Imaging 53(1):223–233. https://doi.org/10.1002/jmri.27335
doi: 10.1002/jmri.27335
Abidi M, de Marco G, Couillandre A, Feron M, Mseddi E, Termoz N, Querin G, Pradat PF, Bede P (2020) Adaptive functional reorganization in amyotrophic lateral sclerosis: coexisting degenerative and compensatory changes. Eur J Neurol 27(1):121–128. https://doi.org/10.1111/ene.14042
doi: 10.1111/ene.14042
Prell T, Grosskreutz J (2013) The involvement of the cerebellum in amyotrophic lateral sclerosis. Amyotroph Lateral Scler Frontotemporal Degener 14(7–8):507–515. https://doi.org/10.3109/21678421.2013.812661
doi: 10.3109/21678421.2013.812661
Bede P, Bogdahn U, Lope J, Chang KM, Xirou S, Christidi F (2021) Degenerative and regenerative processes in amyotrophic lateral sclerosis: motor reserve, adaptation and putative compensatory changes. Neural Regen Res 16(6):1208–1209. https://doi.org/10.4103/1673-5374.300440
doi: 10.4103/1673-5374.300440
Finegan E, Li Hi Shing S, Siah WF, Chipika RH, Chang KM, McKenna MC, Doherty MA, Hengeveld JC, Vajda A, Donaghy C, Hutchinson S, McLaughlin RL, Hardiman O, Bede P (2020) Evolving diagnostic criteria in primary lateral sclerosis: the clinical and radiological basis of “probable PLS.” J Neurol Sci 417:117052. https://doi.org/10.1016/j.jns.2020.117052
doi: 10.1016/j.jns.2020.117052
Finegan E, Chipika RH, Shing SLH, Hardiman O, Bede P (2019) Primary lateral sclerosis: a distinct entity or part of the ALS spectrum? Amyotroph Lateral Scler Frontotemporal Degener 20(3–4):133–145. https://doi.org/10.1080/21678421.2018.1550518
doi: 10.1080/21678421.2018.1550518
El Mendili MM, Querin G, Bede P, Pradat PF (2019) Spinal cord imaging in amyotrophic lateral sclerosis: historical concepts-novel techniques. Front Neurol 10:350. https://doi.org/10.3389/fneur.2019.00350
doi: 10.3389/fneur.2019.00350
pmcid: 6474186
Khamaysa M, Lefort M, Pélégrini-Issac M, Lackmy-Vallée A, Mendili MME, Preuilh A, Devos D, Bruneteau G, Salachas F, Lenglet T, Amador MM, Le Forestier N, Hesters A, Gonzalez J, Rolland AS, Desnuelle C, Chupin M, Querin G, Georges M, Morelot-Panzini C, Marchand-Pauvert V, Pradat PF (2023) Quantitative brainstem and spinal MRI in amyotrophic lateral sclerosis: implications for predicting noninvasive ventilation needs. J Neurol. https://doi.org/10.1007/s00415-023-12045-x
doi: 10.1007/s00415-023-12045-x
Bede P, Bokde AL, Byrne S, Elamin M, Fagan AJ, Hardiman O (2012) Spinal cord markers in ALS: diagnostic and biomarker considerations. Amyotroph Lateral Scler 13(5):407–415. https://doi.org/10.3109/17482968.2011.649760
doi: 10.3109/17482968.2011.649760
Querin G, El Mendili MM, Bede P, Delphine S, Lenglet T, Marchand-Pauvert V, Pradat PF (2018) Multimodal spinal cord MRI offers accurate diagnostic classification in ALS. J Neurol Neurosurg Psychiatry 89(11):1220–1221. https://doi.org/10.1136/jnnp-2017-317214
doi: 10.1136/jnnp-2017-317214
Querin G, Bede P, El Mendili MM, Li M, Pelegrini-Issac M, Rinaldi D, Catala M, Saracino D, Salachas F, Camuzat A, Marchand-Pauvert V, Cohen-Adad J, Colliot O, Le Ber I, Pradat PF (2019) Presymptomatic spinal cord pathology in c9orf72 mutation carriers: a longitudinal neuroimaging study. Ann Neurol 86(2):158–167. https://doi.org/10.1002/ana.25520
doi: 10.1002/ana.25520
Li Hi Shing S, Lope J, McKenna MC, Chipika RH, Hardiman O, Bede P (2021) Increased cerebral integrity metrics in poliomyelitis survivors: putative adaptation to longstanding lower motor neuron degeneration. J Neurol Sci 424:117361. https://doi.org/10.1016/j.jns.2021.117361
doi: 10.1016/j.jns.2021.117361
Li Hi Shing S, Lope J, Chipika RH, Hardiman O, Bede P (2021) Imaging data indicate cerebral reorganisation in poliomyelitis survivors: Possible compensation for longstanding lower motor neuron pathology. Data Brief 38:107316. https://doi.org/10.1016/j.dib.2021.107316
doi: 10.1016/j.dib.2021.107316
pmcid: 8397913
McKenna MC, Chipika RH, Li Hi Shing S, Christidi F, Lope J, Doherty MA, Hengeveld JC, Vajda A, McLaughlin RL, Hardiman O, Hutchinson S, Bede P (2021) Infratentorial pathology in frontotemporal dementia: cerebellar grey and white matter alterations in FTD phenotypes. J Neurol 268(12):4687–4697. https://doi.org/10.1007/s00415-021-10575-w
doi: 10.1007/s00415-021-10575-w
pmcid: 8563547
McKenna MC, Tahedl M, Murad A, Lope J, Hardiman O, Hutchinson S, Bede P (2022) White matter microstructure alterations in frontotemporal dementia: phenotype-associated signatures and single-subject interpretation. Brain Behav 12(2):e2500. https://doi.org/10.1002/brb3.2500
doi: 10.1002/brb3.2500
pmcid: 8865163
Mulkerrin G, França MC Jr, Lope J, Tan EL, Bede P (2022) Neuroimaging in hereditary spastic paraplegias: from qualitative cues to precision biomarkers. Expert Rev Mol Diagn 22(7):745–760. https://doi.org/10.1080/14737159.2022.2118048
doi: 10.1080/14737159.2022.2118048
Bede P, Chang KM, Tan EL (2022) Machine-learning in motor neuron diseases: prospects and pitfalls. Eur J Neurol. https://doi.org/10.1111/ene.15443
doi: 10.1111/ene.15443
pmcid: 9546434
Bede P, Murad A, Hardiman O (2021) Pathological neural networks and artificial neural networks in ALS: diagnostic classification based on pathognomonic neuroimaging features. J Neurol. https://doi.org/10.1007/s00415-021-10801-5
doi: 10.1007/s00415-021-10801-5
pmcid: 9021106
Bede P, Murad A, Lope J, Li Hi Shing S, Finegan E, Chipika RH, Hardiman O, Chang KM (2021) Phenotypic categorisation of individual subjects with motor neuron disease based on radiological disease burden patterns: a machine-learning approach. J Neurol Sci 432:120079. https://doi.org/10.1016/j.jns.2021.120079
doi: 10.1016/j.jns.2021.120079
Bede P, Pradat PF, Lope J, Vourc’h P, Blasco H, Corcia P (2022) Primary lateral sclerosis: clinical, radiological and molecular features. Rev neurol 178(3):196–205. https://doi.org/10.1016/j.neurol.2021.04.008
doi: 10.1016/j.neurol.2021.04.008
Feron M, Couillandre A, Mseddi E, Termoz N, Abidi M, Bardinet E, Delgadillo D, Lenglet T, Querin G, Welter ML, Le Forestier N, Salachas F, Bruneteau G, Del Mar AM, Debs R, Lacomblez L, Meininger V, Pelegrini-Issac M, Bede P, Pradat PF, de Marco G (2018) Extrapyramidal deficits in ALS: a combined biomechanical and neuroimaging study. J Neurol 265(9):2125–2136. https://doi.org/10.1007/s00415-018-8964-y
doi: 10.1007/s00415-018-8964-y