The CCAS-scale in hereditary ataxias: helpful on the group level, particularly in SCA3, but limited in individual patients.
Bedside test
Cerebellum
FRDA
SCA3
SCA6
Journal
Journal of neurology
ISSN: 1432-1459
Titre abrégé: J Neurol
Pays: Germany
ID NLM: 0423161
Informations de publication
Date de publication:
Aug 2022
Aug 2022
Historique:
received:
11
11
2021
accepted:
23
02
2022
revised:
22
02
2022
pubmed:
3
4
2022
medline:
22
7
2022
entrez:
2
4
2022
Statut:
ppublish
Résumé
A brief bedside test has recently been introduced by Hoche et al. (Brain, 2018) to screen for the Cerebellar Cognitive Affective Syndrome (CCAS) in patients with cerebellar disease. This multicenter study tested the ability of the CCAS-Scale to diagnose CCAS in individual patients with common forms of hereditary ataxia. A German version of the CCAS-Scale was applied in 30 SCA3, 14 SCA6 and 20 FRDA patients, and 64 healthy participants matched for age, sex, and level of education. Based on original cut-off values, the number of failed test items was assessed, and CCAS was considered possible (one failed item), probable (two failed items) or definite (three failed items). In addition a total sum raw score was calculated. On a group level, failed items were significantly higher and total sum scores were significantly lower in SCA3 patients compared to matched controls. SCA6 and FRDA patients performed numerically below controls, but respective group differences failed to reach significance. The ability of the CCAS-Scale to diagnose CCAS in individual patients was limited to severe cases failing three or more items. Milder cases failing one or two items showed a great overlap with the performance of controls exhibiting a substantial number of false-positive test results. The word fluency test items differentiated best between patients and controls. As a group, SCA3 patients performed below the level of SCA6 and FRDA patients, possibly reflecting additional cerebral involvement. Moreover, the application of the CCAS-Scale in its present form results in a high number of false-positive test results, that is identifying controls as patients, reducing its usefulness as a screening tool for CCAS in individual patients.
Sections du résumé
BACKGROUND
BACKGROUND
A brief bedside test has recently been introduced by Hoche et al. (Brain, 2018) to screen for the Cerebellar Cognitive Affective Syndrome (CCAS) in patients with cerebellar disease.
OBJECTIVE
OBJECTIVE
This multicenter study tested the ability of the CCAS-Scale to diagnose CCAS in individual patients with common forms of hereditary ataxia.
METHODS
METHODS
A German version of the CCAS-Scale was applied in 30 SCA3, 14 SCA6 and 20 FRDA patients, and 64 healthy participants matched for age, sex, and level of education. Based on original cut-off values, the number of failed test items was assessed, and CCAS was considered possible (one failed item), probable (two failed items) or definite (three failed items). In addition a total sum raw score was calculated.
RESULTS
RESULTS
On a group level, failed items were significantly higher and total sum scores were significantly lower in SCA3 patients compared to matched controls. SCA6 and FRDA patients performed numerically below controls, but respective group differences failed to reach significance. The ability of the CCAS-Scale to diagnose CCAS in individual patients was limited to severe cases failing three or more items. Milder cases failing one or two items showed a great overlap with the performance of controls exhibiting a substantial number of false-positive test results. The word fluency test items differentiated best between patients and controls.
CONCLUSIONS
CONCLUSIONS
As a group, SCA3 patients performed below the level of SCA6 and FRDA patients, possibly reflecting additional cerebral involvement. Moreover, the application of the CCAS-Scale in its present form results in a high number of false-positive test results, that is identifying controls as patients, reducing its usefulness as a screening tool for CCAS in individual patients.
Identifiants
pubmed: 35364683
doi: 10.1007/s00415-022-11071-5
pii: 10.1007/s00415-022-11071-5
pmc: PMC9293809
doi:
Types de publication
Journal Article
Multicenter Study
Langues
eng
Sous-ensembles de citation
IM
Pagination
4363-4374Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : FU356/12-1
Organisme : Deutsche Forschungsgemeinschaft
ID : 441409627
Organisme : European Joint Programme on Rare Diseases
ID : 825575
Organisme : German Heredoataxia Societey
Organisme : Freunde and Förderer der Neurologie am Universitätsklinikum Essen
Informations de copyright
© 2022. The Author(s).
Références
Schmahmann JD, Sherman JC (1997) Cerebellar cognitive affective syndrome. Int Rev Neurobiol 41:433–440. https://doi.org/10.1016/s0074-7742(08)60363-3
doi: 10.1016/s0074-7742(08)60363-3
pubmed: 9378601
Schmahmann JD, Sherman JC (1998) The cerebellar cognitive affective syndrome. Brain 121:561–579. https://doi.org/10.1093/brain/121.4.561
doi: 10.1093/brain/121.4.561
pubmed: 9577385
Hoche F, Guell X, Vangel MG, Sherman JC, Schmahmann JD (2018) The cerebellar cognitive affective/ Schmahmann syndrome scale. Brain 141:248–270. https://doi.org/10.1093/brain/awx317
doi: 10.1093/brain/awx317
pubmed: 29206893
King M, Hernandez-Castillo CR, Poldrack RA, Ivry RB, Diedrichsen J (2019) Functional boundaries in the human cerebellum revealed by a multi-domain task battery. Nat Neurosci 22:1371–1378. https://doi.org/10.1038/s41593-019-0436-x
doi: 10.1038/s41593-019-0436-x
pubmed: 31285616
pmcid: 8312478
Adamaszek M, D’Agata F, Ferrucci R, Habas C, Keulen S, Kirkby KC, Leggio M, Marien P, Molinari M, Moulton E, Orsi L, Van Overwalle F, Papadelis C, Priori A, Sacchetti B, Schutter DJ, Styliadis C, Verhoeven J (2017) Consensus paper: cerebellum and emotion. Cerebellum 16:552–576. https://doi.org/10.1007/s12311-016-0815-8
doi: 10.1007/s12311-016-0815-8
pubmed: 27485952
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 19:102–125. https://doi.org/10.1007/s12311-019-01068-8
doi: 10.1007/s12311-019-01068-8
pubmed: 31522332
Jacobi H, Faber J, Timmann D, Klockgether T (2021) Update cerebellum and cognition. J Neurol 268:3921–3925. https://doi.org/10.1007/s00415-021-10486-w
doi: 10.1007/s00415-021-10486-w
pubmed: 33656586
pmcid: 8463403
Guell X, Gabrieli JDE, Schmahmann JD (2018) Triple representation of language, working memory, social and emotion processing in the cerebellum: convergent evidence from task and seed-based resting-state fMRI analyses in a single large cohort. Neuroimage 172:437–449. https://doi.org/10.1016/j.neuroimage.2018.01.082
doi: 10.1016/j.neuroimage.2018.01.082
pubmed: 29408539
Globas C, Bosch S, Zuhlke C, Daum I, Dichgans J, Burk K (2003) The cerebellum and cognition. Intellectual function in spinocerebellar ataxia type 6 (SCA6). J Neurol 250:1482–1487. https://doi.org/10.1007/s00415-003-0258-2
doi: 10.1007/s00415-003-0258-2
pubmed: 14673583
Dogan I, Tinnemann E, Romanzetti S, Mirzazade S, Costa AS, Werner CJ, Heim S, Fedosov K, Schulz S, Timmann D, Giordano IA, Klockgether T, Schulz JB, Reetz K (2016) Cognition in Friedreich’s ataxia: a behavioral and multimodal imaging study. Ann Clin Transl Neurol 3:572–587. https://doi.org/10.1002/acn3.315
doi: 10.1002/acn3.315
pubmed: 27606341
pmcid: 4999591
Garrard P, Martin NH, Giunti P, Cipolotti L (2008) Cognitive and social cognitive functioning in spinocerebellar ataxia : a preliminary characterization. J Neurol 255:398–405. https://doi.org/10.1007/s00415-008-0680-6
doi: 10.1007/s00415-008-0680-6
pubmed: 18350360
Cooper FE, Grube M, Von Kriegstein K, Kumar S, English P, Kelly TP, Chinnery PF, Griffiths TD (2012) Distinct critical cerebellar subregions for components of verbal working memory. Neuropsychologia 50:189–197. https://doi.org/10.1016/j.neuropsychologia.2011.11.017
doi: 10.1016/j.neuropsychologia.2011.11.017
pubmed: 22133495
Suenaga M, Kawai Y, Watanabe H, Atsuta N, Ito M, Tanaka F, Katsuno M, Fukatsu H, Naganawa S, Sobue G (2008) Cognitive impairment in spinocerebellar ataxia type 6. J Neurol Neurosurg Psychiatry 79:496–499. https://doi.org/10.1136/jnnp.2007.119883
doi: 10.1136/jnnp.2007.119883
pubmed: 17682009
Kawai Y, Suenaga M, Watanabe H, Sobue G (2009) Cognitive impairment in spinocerebellar degeneration. Eur Neurol 61:257–268. https://doi.org/10.1159/000206850
doi: 10.1159/000206850
pubmed: 19295212
Schmitz-Huebsch T, Coudert M, Tezenas du Montcel S, Giunti P, Labrum R, Durr A, Ribai P, Charles P, Linnemann C, Schoels L, Rakowicz M, Rola R, Zdzienicka E, Fancellu R, Mariotti C, Baliko L, Melegh B, Filla A, Salvatore E, van de Warrenburg BP, Szymanski S, Infante J, Timmann D, Boesch S, Depondt C, Kang JS, Schulz JB, Klopstock T, Lossnitzer N, Lowe B, Frick C, Rottlander D, Schlaepfer TE, Klockgether T (2011) Depression comorbidity in spinocerebellar ataxia. Mov Disord 26:870–876. https://doi.org/10.1002/mds.2369
doi: 10.1002/mds.2369
Nieto A, Correia R, de Nóbrega E, Montón F, Hess S, Barroso J (2012) Cognition in Friedreich ataxia. Cerebellum 11:834–844. https://doi.org/10.1007/s12311-012-0363-9
doi: 10.1007/s12311-012-0363-9
pubmed: 22351352
Zawacki TM, Grace J, Friedman JH, Sudarsky L (2002) Executive and emotional dysfunction in Machado-Joseph disease. Mov Disord 17:1004–1010. https://doi.org/10.1002/mds.10033
doi: 10.1002/mds.10033
pubmed: 12360550
Lopes TM, D’Abreu A, França MC, Yasuda CL, Betting LE, Samara AB, Castellano G, Somazz JC, Balthazar ML, Lopes-Cendes I, Cendes F (2013) Widespread neuronal damage and cognitive dysfunction in spinocerebellar ataxia type 3. J Neurol 260:2370–2379. https://doi.org/10.1007/s00415-013-6998-8
doi: 10.1007/s00415-013-6998-8
pubmed: 23775343
Klinke I, Minnerop M, Schmitz-Hübsch T, Hendriks M, Klockgether T, Wüllner U, Helmstaedter C (2010) Neuropsychological features of patients with spinocerebellar ataxia (SCA) types 1, 2, 3, and 6. Cerebellum 9:433–442. https://doi.org/10.1007/s12311-010-0183-8
doi: 10.1007/s12311-010-0183-8
pubmed: 20502998
pmcid: 2949561
Ma J, Wu C, Lei J, Zhang X (2014) Cognitive impairments in patients with spinocerebellar ataxia types 1, 2 and 3 are positively correlated to the clinical severity of ataxia symptoms. Int J Clin Exp Med 7:5765–5771
pubmed: 25664104
pmcid: 4307551
D’Agata F, Caroppo P, Baudino B, Caglio M, Croce M, Bergui M, Tamietto M, Mortara P, Orsi L (2011) The recognition of facial emotions in spinocerebellar ataxia patients. Cerebellum 10:600–610. https://doi.org/10.1007/s12311-011-0276-z
doi: 10.1007/s12311-011-0276-z
pubmed: 21503592
Nieto A, Hernández-Torres A, Pérez-Flores J, Montón F (2018) Depressive symptoms in Friedreich ataxia. Int J Clin Health Psychol 18:18–26. https://doi.org/10.1016/j.ijchp.2017.11.004
doi: 10.1016/j.ijchp.2017.11.004
pubmed: 30487906
Braga-Neto P, Dutra LA, Pedroso JL, Felício AC, Alessi H, Santos-Galduroz RF, Bertolucci PH, Castiglioni ML, Bressan RA, de Garrido GE, Barsottini OG, Jackowski A (2012) Cognitive deficits in Machado-Joseph disease correlate with hypoperfusion of visual system areas. Cerebellum 11:1037–1044. https://doi.org/10.1007/s12311-012-0354-x
doi: 10.1007/s12311-012-0354-x
pubmed: 22307858
Kawai Y, Takeda A, Abe Y, Washimi Y, Tanaka F, Sobue G (2004) Cognitive impairments in Machado-Joseph disease. Arch Neurol 61:1757–1760. https://doi.org/10.1001/archneur.61.11.1757
doi: 10.1001/archneur.61.11.1757
pubmed: 15534186
Cocozza S, Costabile T, Pontillo G, Lieto M, Russo C, Radice L, Pane C, Filla A, Brunetti A, Saccà F (2020) Cerebellum and cognition in Friedreich ataxia: a voxel-based morphometry and volumetric MRI study. J Neurol 267:350–358. https://doi.org/10.1007/s00415-019-09582-9
doi: 10.1007/s00415-019-09582-9
pubmed: 31641877
Nieto A, Correia R, de Nóbrega E, Montón F, Barroso J (2013) Cognition in late-onset Friedreich ataxia. Cerebellum 12:504–512. https://doi.org/10.1007/s12311-013-0457-z
doi: 10.1007/s12311-013-0457-z
pubmed: 23397368
Roeske S, Filla I, Heim S, Amunts K, Helmstaedter C, Wüllner U, Wagner M, Klockgether T, Minnerop M (2013) Progressive cognitive dysfunction in spinocerebellar ataxia type 3. Mov Disord 28:1435–1438. https://doi.org/10.1002/mds.25512
doi: 10.1002/mds.25512
pubmed: 23736996
Tamura I, Takei A, Hamada S, Nonaka M, Kurosaki Y, Moriwaka F (2017) Cognitive dysfunction in patients with spinocerebellar ataxia type 6. J Neurol 264:260–267. https://doi.org/10.1007/s00415-016-8344-4
doi: 10.1007/s00415-016-8344-4
pubmed: 27878440
Rentiya Z, Khan NS, Ergun E, Ying SH, Desmond JE (2017) Distinct cerebellar regions related to motor and cognitive performance in SCA6 patients. Neuropsychologia 107:25–30. https://doi.org/10.1016/j.neuropsychologia.2017.10.036
doi: 10.1016/j.neuropsychologia.2017.10.036
pubmed: 29100951
pmcid: 5705404
Selvadurai LP, Harding IH, Corben LA, Stagnitti MR, Storey E, Egan GF, Delatycki MB, Georgiou-Karistianis N (2016) Cerebral and cerebellar grey matter atrophy in Friedreich ataxia: the IMAGE-FRDA study. J Neurol 263:2215–2223. https://doi.org/10.1007/s00415-016-8252-7
doi: 10.1007/s00415-016-8252-7
pubmed: 27522354
Yap KH, Kessels RPC, Azmin S, van de Warrenburg B, Mohamed Ibrahim N (2021) Neurocognitive changes in spinocerebellar ataxia type 3: a systematic review with a narrative design. Cerebellum: Epub ahead of print. https://doi.org/10.1007/s12311-021-01282-3
Thieme A, Roeske S, Faber J, Sulzer P, Minnerop M, Elben S, Jacobi H, Reetz K, Dogan I, Barkhoff M, Konczak J, Wondzinski E, Siebler M, Mueller O, Sure U, Schmahmann JD, Klockgether T, Synofzik M, Timmann D (2020) Validation of a German version of the Cerebellar Cognitive Affective/ Schmahmann Syndrome Scale: preliminary version and study protocol. Neurol Res Pract 2:39. https://doi.org/10.1186/s42466-020-00071-3
doi: 10.1186/s42466-020-00071-3
pubmed: 33324939
pmcid: 7650062
Rodríguez-Labrada R, Batista-Izquierdo A, González-Melix Z, Reynado-Cejas L, Vázquez- Mojena Y, Sanz YA, Canales-Ochoa N, González-Zaldívar Y, Dogan I, Reetz K, Velázquez- Pérez L (2021) Cognitive decline is closely associated with ataxia severity in Spinocerebellar Ataxia Type 2: a Validation Study of the Schmahmann Syndrome Scale. Cerebellum: Epub ahead of print. https://doi.org/10.1007/s12311-021-01305-z
Maas RPPW, Killaars S, van de Warrenburg BPC, Schutter DJLG (2021) The cerebellar cognitive affective syndrome scale reveals early neuropsychological deficits in SCA3 patients. J Neurol 268:3456–3466. https://doi.org/10.1007/s00415-021-10516-7
doi: 10.1007/s00415-021-10516-7
pubmed: 33743045
pmcid: 8357713
Stephen CD, Balkwill D, James P, Haxton E, Sassower K, Schmahmann JD, Eichler F, Lewis R (2020) Quantitative oculomotor and nonmotor assessments in late-onset GM2 gangliosidosis. Neurology 94:e705–e717. https://doi.org/10.1212/WNL.0000000000008959
doi: 10.1212/WNL.0000000000008959
pubmed: 31964693
pmcid: 7176300
Chirino-Pérez A, Marrufo-Meléndez OR, Muñoz-López JI, Hernandez-Castillo CR, Ramirez- Garcia G, Díaz R, Nuñez-Orozco L, Fernandez-Ruiz J (2021) Mapping the cerebellar cognitive affective syndrome in patients with chronic cerebellar strokes. Cerebellum: Epub ahead of print. https://doi.org/10.1007/s12311-021-01290-3
Naeije G, Rai M, Allaerts N, Sjogard M, De Tiège X, Pandolfo M (2020) Cerebellar cognitive disorder parallels cerebellar motor symptoms in Friedreich ataxia. Ann Clin Transl Neurol 7:1050–1054. https://doi.org/10.1002/acn3.51079
doi: 10.1002/acn3.51079
pubmed: 32510804
pmcid: 7317641
Thieme A, Röske S, Faber J, Sulzer P, Minnerop M, Elben S, Reetz K, Dogan I, Barkhoff M, Konczak J, Wondzinski E, Siebler M, Hetze S, Müller O, Sure U, Klockgether T, Synofzik M, Timmann D (2021) Reference values for the cerebellar cognitive affective syndrome scale: age and education matter. Brain 144:e20. https://doi.org/10.1093/brain/awaa41
doi: 10.1093/brain/awaa41
pubmed: 33367632
Schmitz-Huebsch T, du Montcel ST, Baliko L, Berciano J, Boesch S, Depondt C, Giunti P, Globas C, Infante J, Kang JS, Kremer B, Mariotti C, Melegh B, Pandolfo M, Rakowicz M, Ribai P, Rola R, Schoels L, Szymanski S, van de Warrenburg BP, Durr A, Klockgether T, Fancellu R (2006) Scale for the assessment and rating of ataxia: development of a new clinical scale. Neurology 66:1717–1720. https://doi.org/10.1212/01.wnl.0000219042.60538.92
doi: 10.1212/01.wnl.0000219042.60538.92
Jacobi H, Rakowicz M, Rola R, Fancellu R, Mariotti C, Charles P, Durr A, Kueper M, Timmann D, Linnemann C, Schoels L, Kaut O, Schaub C, Filla A, Baliko L, Melegh B, Kang JS, Giunti P, van de Warrenburg BP, Fimmers R, Klockgether T (2013) Inventory of Non-Ataxia Signs (INAS): validation of a new clinical assessment instrument. Cerebellum 12:418–428. https://doi.org/10.1007/s12311-012-0421-3
doi: 10.1007/s12311-012-0421-3
pubmed: 23090211
Ho J, Tumkaya T, Aryal S, Choi H, Claridge-Chang A (2019) Moving beyond P values: data analysis with estimation graphics. Nat Methods 16:565–566. https://doi.org/10.1038/s41592-019-0470-3
doi: 10.1038/s41592-019-0470-3
pubmed: 31217592
Van der Schouw YT, Verbeek AL, Ruijs JH (1992) ROC curves for the initial assessment of new diagnostic tests. Fam Pract 9:506–511. https://doi.org/10.1093/fampra/9.4.506
doi: 10.1093/fampra/9.4.506
pubmed: 1490547
D’Agostino RB, Pencina MJ, Massaro JM, Coady S (2013) Cardiovascular disease risk assessment: insights from Framingham. Glob Heart 8:11–23. https://doi.org/10.1016/j.gheart.2013.01.001
doi: 10.1016/j.gheart.2013.01.001
pubmed: 23750335
Faletti R, Battisti G, Discalzi A, Grognardi ML, Martinello S, Oderda M, Gontero P, Bergamasco L, Cassinis MC, Fonio P (2016) Can DW-MRI, with its ADC values, be a reliable predictor of biopsy outcome in patients with suspected prostate cancer? Abdom Radiol (NY) 41:926–933. https://doi.org/10.1007/s00261-015-0574-x
doi: 10.1007/s00261-015-0574-x
Terwee CB, Bot SD, de Boer MR, van der Windt DA, Knol DL, Dekker J, Bouter LM, de Vet HC (2007) Quality criteria were proposed for measurement properties of health status questionnaires. J Clin Epidemiol 60:34–42. https://doi.org/10.1016/j.jclinepi.2006.03.012
doi: 10.1016/j.jclinepi.2006.03.012
pubmed: 17161752
Youden WJ (1950) Index for rating diagnostic tests. Cancer 3:32–35. https://doi.org/10.1002/1097-0142(1950)3:1%3c32:aid-cncr2820030106%3e3.0.co;2-3
doi: 10.1002/1097-0142(1950)3:1<32:aid-cncr2820030106>3.0.co;2-3
pubmed: 15405679
Braga-Neto P, Pedroso JL, Alessi H, Dutra LA, Felicio AC, Minett T, Weisman P, Santos-Galduroz RF, Bertolucci PH, Gabbai AA, Barsottini OG (2012) Cerebellar cognitive affective syndrome in Machado Joseph disease: core clinical features. Cerebellum 11:549–556. https://doi.org/10.1007/s12311-011-0318-6
doi: 10.1007/s12311-011-0318-6
pubmed: 21975858
Strick PL, Dum RP, Fiez JA (2009) Cerebellum and nonmotor function. Annu Rev Neurosci 32:413–434. https://doi.org/10.1146/annurev.neuro.31.060407.125606
doi: 10.1146/annurev.neuro.31.060407.125606
pubmed: 19555291
Palesi F, Ferrante M, Gaviraghi M, Misiti A, Savini G, Lascialfari A, D’Angelo E, Gandini Wheeler-Kingshott CAM (2021) Motor and higher-order functions topography of the human dentate nuclei identified with tractography and clustering methods. Hum Brain Mapp 42:4348–4361. https://doi.org/10.1002/hbm.25551
doi: 10.1002/hbm.25551
pubmed: 34087040
pmcid: 8356999
Tedesco AM, Chiricozzi FR, Clausi S, Lupo M, Molinari M, Leggio MG (2011) The cerebellar cognitive profile. Brain 134:3672–3686. https://doi.org/10.1093/brain/awr266
doi: 10.1093/brain/awr266
pubmed: 22036960
Koeppen AH, Ramirez RL, Bjork ST, Bauer P, Feustel PJ (2013) The reciprocal cerebellar circuitry in human hereditary ataxia. Cerebellum 12:493–503. https://doi.org/10.1007/s12311-013-0456-0
doi: 10.1007/s12311-013-0456-0
pubmed: 23389921
pmcid: 3700561
Bidichandani SI, Delatycki MB (1993–2021) Friedreich Ataxia. In: Adam MP, Ardinger HH, Pagon RA, Wallace SE, Bean LJH, Stephens K, Amemiya A (eds) Gene Reviews [Internet]
Stefanescu MR, Dohnalek M, Maderwald S, Thürling M, Minnerop M, Beck A, Schlamann M, Diedrichsen J, Ladd ME, Timmann D (2015) Structural and functional MRI abnormalities of cerebellar cortex and nuclei in SCA3, SCA6 and Friedreich’s ataxia. Brain 138:1182–1197. https://doi.org/10.1093/brain/awv064
doi: 10.1093/brain/awv064
pubmed: 25818870
pmcid: 5963415
Hernández-Torres A, Montón F, Hess Medler S, de Nóbrega É, Nieto A (2021) Longitudinal study of cognitive functioning in Friedreich’s Ataxia. J Int Neuropsychol Soc 27:343–350. https://doi.org/10.1017/S1355617720000958
doi: 10.1017/S1355617720000958
pubmed: 33050966
Sayah S, Rotgé JY, Francisque H, Gargiulo M, Czernecki V, Justo D, Lahlou-Laforet K, Hahn V, Pandolfo M, Pelissolo A, Fossati P, Durr A (2018) Personality and neuropsychological profiles in Friedreich Ataxia. Cerebellum 17:204–212. https://doi.org/10.1007/s12311-017-0890-5
doi: 10.1007/s12311-017-0890-5
pubmed: 29086357
Giocondo F, Curcio G (2018) Spinocerebellar ataxia: a critical review of cognitive and sociocognitive deficits. Int J Neurosci 128:182–191. https://doi.org/10.1080/00207454.2017.1377198
doi: 10.1080/00207454.2017.1377198
pubmed: 28877638
Van Overwalle F, De Coninck S, Heleven E, Perrotta G, Taib NOB, Manto M, Marien P (2019) The role of the cerebellum in reconstructing social action sequences: a pilot study. Soc Cogn Affect Neurosci 14:549–558. https://doi.org/10.1093/scan/nsz032
doi: 10.1093/scan/nsz032
pubmed: 31037308
pmcid: 6545532
Shishegar R, Harding IH, Corben LA, Delatycki MB, Storey E, Egan GF, Georgiou-Karistianis N (2020) Longitudinal increases in cerebral brain activation during working memory performance in Friedreich Ataxia: 24-month data from IMAGE-FRDA. Cerebellum 19:182–191. https://doi.org/10.1007/s12311-019-01094-6
doi: 10.1007/s12311-019-01094-6
pubmed: 31898277