Are Socio-Affective Impairments in Ataxia Related to Language and Processing Speed Deficits?

Main Article Content

Claudine Mélan Noëlie Renaudié

Abstract

Over the last decade a number of studies have demonstrated the implication of the cerebellum in cognition, including verbal memory, executive function, and language. Social cognition abilities like emotion attribution and theory of mind are essential in social interaction and rely on verbal abilities and executive functions. Involvement in social cognition has been explored in the most common forms of Spinocerebellar Ataxia (SCA), but several aspects remain unclear. The present study tested whether socio-affective impairments are observed in SCA patients by using different tasks and to determine whether these impairments were associated with reduced verbal processing and/or processing speed. 13 patients (SCA1, n=1; SC2, n=5; SCA3, n=7) were matched with 13 controls for gender, age and education. Verbal and non-verbal theory of mind abilities were tested (validated French versions of an attribution of intention test, faux-pas test), and emotion attribution. Language efficacy was explored in a word fluency test and processing speed in two non-motor tasks. Results revealed no difference between SCA2 and SCA3 patients in neither socio-affective nor cognitive test. Performance on all tests was on contrary significantly reduced in the SCA patient group compared to controls. SCA patients’ performance was positively correlated between the three social cognition tests, indicating a somewhat generalized impairment. Their performance rate in each of three social cognition tests was further correlated with processing speed but not with word fluency. In the verbal theory of mind task they displayed however comprehension deficits of the faux-pas and of general control questions. Taken together the data suggest that processing speed and comprehension difficulties might account, partly at least, for socio-affective and cognitive deficits in both genotypes. This conclusion was modulated by the observation that the neuropsychological features did not correspond well with age of illness diagnosis and illness duration, indicating that there is a degree of heterogeneity in the cognitive profiles and social cognitive impairments in SCA patients.

Keywords: Theory of mind, emotion attribution, cognitive speed, fluency, SCA2, SCA3

Article Details

How to Cite
MÉLAN, Claudine; RENAUDIÉ, Noëlie. Are Socio-Affective Impairments in Ataxia Related to Language and Processing Speed Deficits?. Medical Research Archives, [S.l.], v. 9, n. 10, oct. 2021. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/2563>. Date accessed: 25 apr. 2024. doi: https://doi.org/10.18103/mra.v9i10.2563.
Section
Research Articles

References

1. Schmahmann JD. An emerging concept. The cerebellar contribution to higher function. Arch Neurol. 1991 Nov;48(11):1178-87. doi: 10.1001/archneur.1991.00530230086029
2. Manto MU. The wide spectrum of spinocerebellar ataxias (SCAs). Cerebellum. 2005;4(1):2–6. doi: 10.1080/14734220510007914
3. Gambardella A, Annesi G, Bono F, Spadafora P, Valentino P, Pasqua AA, Mazzei R, Montesanti R, Conforti FL, Oliveri RL, Zappia M, Aguglia U, Quattrone A. CAG repeat length and clinical features in three Italian families with spinocerebellar ataxia type 2 (SCA2): early impairment of Wisconsin Card Sorting Test and saccade velocity. J Neurol. 1998 Oct;245(10):647-52. doi: 10.1007/s004150050261
4. Le Pira F, Zappalà G, Saponara R, Domina E, Restivo D, Reggio E, Nicoletti A, Giuffrida S. Cognitive findings in spinocerebellar ataxia type 2: relationship to genetic and clinical variables. J Neurol Sci. 2002 Sep 15;201(1-2):53-7. doi: 10.1016/s0022-510x(02)00194-6
5. Sokolovsky N, Cook A, Hunt H, Giunti P, Cipolotti L. A preliminary characterisation of cognition and social cognition in spinocerebellar ataxia types 2, 1, and 7. Behav Neurol. 2010;23(1-2):17-29. doi: 10.3233/BEN-2010-0270
6. Bürk K, Globas C, Bösch S, Klockgether T, Zühlke C, Daum I, Dichgans J. Cognitive deficits in spinocerebellar ataxia type 1, 2, and 3. J Neurol. 2003 Feb;250(2):207-11. doi: 10.1007/s00415-003-0976-5
7. D'Agata F, Caroppo P, Baudino B, Caglio M, Croce M, Bergui M et al. The recognition of facial emotions in spinocerebellar ataxia patients. Cerebellum 2011;10(3):600-610. doi.org/10.1007/s12311-011-0276-z
8. Moriarty A, Cook A, Hunt H, Adams ME, Cipolotti L, Giunti P. A longitudinal investigation into cognition and disease progression in spinocerebellar ataxia types 1, 2, 3, 6, and 7. Orphanet J Rare Dis. 2016 Jun 22;11(1):82. doi: 10.1186/s13023-016-0447-6
9. Storey E, Forrest SM, Shaw JH, Mitchell P, Gardner RJM. Spinocerebellar Ataxia Type 2: Clinical Features of a Pedigree Displaying Prominent Frontal-Executive Dysfunction. Arch Neurol. 1999;56(1):43–50. doi:10.1001/archneur.56.1.43
10. Garrard P, Martin NH, Giunti P, Cipolotti L. Cognitive and social cognitive functioning in spinocerebellar ataxia: a preliminary characterization. J Neurol. 2008;255(3):398–405. doi:10.1007/s00415-008-0680-6
11. Baron-Cohen S, Wheelwright S, Hill J, Raste Y, Plump I. The ‘‘Reading the Mind in the Eyes’’ Test Revised Version: A Study with Normal Adults, and Adults with Asperger Syndrome or High-functioning Autism. J. Child Psychol. Psychiat. 2001;42(2):241-251. doi.org/10.1111/1469-7610.00715
12. Olivito G, Cercignani M, Lupo M, Iacobacci C, Clausi S, Romano S, Masciullo M, Molinari M, Bozzali M, Leggio M. Neural substrates of motor and cognitive dysfunctions in SCA2 patients: A network based statistics analysis. Neuroimage Clin. 2017 Mar 25;14:719-725. doi: 10.1016/j.nicl.2017.03.009
13. Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BT. The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol. 2011 Nov;106(5):2322-45. doi: 10.1152/jn.00339.2011
14. Brunet E, Sarfati Y, Hardy-Baylé MC, Decety J. A PET investigation of the attribution of intentions with a nonverbal task. Neuroimage 2000 Feb;11(2):157-66. doi: 10.1006/nimg.1999.0525
15. Calarge C, Andreasen NC, O'Leary DS. Visualizing how one brain understands another: a PET study of theory of mind. Am J Psychiatry. 2003 Nov;160(11):1954-64. doi: 10.1176/appi.ajp.160.11.1954
16. Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage 2009 Jan 15;44(2):489-501. doi: 10.1016/j.neuroimage.2008.08.039
17. Schutter DJ, Enter D, Hoppenbrouwers SS. High-frequency repetitive transcranial magnetic stimulation to the cerebellum and implicit processing of happy facial expressions. J Psychiatry Neurosci. 2009 Jan;34(1):60-5.
18. Abel CG, Stein G, Galarregui M, Garretto N, Mangone C, Genovese O et al. Social cognition and theory of mind assessment in nondemented patients with isolated cerebellar degeneration. Arquivos de Neuro-Psiquiatria. 2007;65(2A):304–312. doi: 10.1590/S0004-282X2007000200022
19. Mothersill O, Knee-Zaska C, Donohoe G. Emotion and Theory of Mind in Schizophrenia-Investigating the Role of the Cerebellum. Cerebellum 2016;15(3):357-68. doi: 10.1007/s12311-015-0696-2
20. Andreasen NC, Calarge CA, O'Leary DS. Theory of mind and schizophrenia: a positron emission tomography study of medication-free patients. Schizophr Bull. 2008;34(4):708-19. doi: 10.1093/schbul/sbn034
21. Brady RO Jr, Beermann A, Nye M, Eack SM, Mesholam-Gately R, Keshavan M, Lewandowski KE. Cerebellar-Cortical Connectivity Is Linked to Social Cognition Trans-Diagnostically. Front. Psychiatry. 2020 Nov11:573002. doi: 10.3389/fpsyt.2020.573002
22. Samson D, Houthuys S, Humphreys GW. Self-perspective inhibition deficits cannot beexplained by general executive control difficulties. Cortex 2015;70,189-201. doi:10.1016/j.cortex.2014.12.021
23. Verhaeghen P. Aging and executive control: reports of a demise greatly exaggerated. Curr. Dir. Psychol. Sci. 2011;20 (3), 174–180. doi: 10.1177/0963721411408772
24. Stavroussi P, Andreou G, Karagiannopoulou D. Verbal Fluency and Verbal Short-Term Memory in Adults with Down Syndrome and Unspecified Intellectual Disability. Int J Disabil Dev Educ. 2016;63(1),1-18. doi:10.1080/1034912X.2015.1111307
25. Bolton C, Lacy M. Comparison of cognitive profiles in spinocerebellar ataxia subtypes: a case series. Cerebellum Ataxias. 2019 Sep;6:13. doi: 10.1186/s40673-019-0107-4
26. Meles SK, Kok JG, De Jong BM, Renken RJ, de Vries JJ, Spikman JM, Ziengs AL, Willemsen AT, van der Horn HJ, Leenders KL, Kremer HP. The cerebral metabolic topography of spinocerebellar ataxia type 3. Neuroimage Clin. 2018 Mar; 19:90 - 97. doi: 10.1016/j.nicl.2018.03.038
27. Slapik M, Kronemer SI, Morgan O, Bloes R, Lieberman S, Mandel J, Rosenthal L, Marvel C. Visuospatial Organization and Recall in Cerebellar Ataxia. Cerebellum 2019 Feb;18(1):33-46. doi: 10.1007/s12311-018-0948-z
28. Pedersen A, Koelkebeck K, Brandt M, Wee M, Kueppers KA, Kugel H, Kohl W, Bauer J, Ohrmann P. Theory of mind in patients with schizophrenia: is mentalizing delayed? Schizophr Res. 2012 May;137(1-3):224-9. doi: 10.1016/j.schres.2012.02.022
29. Le Pira F, Giuffrida S, Maci T, Marturano L, Tarantello R, Zappalà G, Nicoletti A, Zappia M. Dissociation between motor and cognitive impairments in SCA2: Evidence from a follow-up study. J Neurol. 2007;254(10),1455–6. doi:10.1007/s00415-007-0548-1
30. Schmitz-Hübsch T, Coudert M, Bauer P, Giunti P, Globas C, Baliko L, Filla A, Mariotti C, Rakowicz M, Charles P, Ribai P, Szymanski S, Infante J, van de Warrenburg BP, Dürr A, Timmann D, Boesch S, Fancellu R, Rola R, Depondt C, Schöls L, Zdienicka E, Kang JS, Döhlinger S, Kremer B, Stephenson DA, Melegh B, Pandolfo M, di Donato S, du Montcel ST, Klockgether T. Spinocerebellar ataxia types 1, 2, 3, and 6: disease severity and nonataxia symptoms. Neurology 2008 Sep 23;71(13):982-9. doi: 10.1212/01.wnl.0000325057.33666.72
31. Burger L, Fay S, Angel L, Borella E, Noiret N, Plusquellec P, Taconnat L. Benefit of Practice of the Stroop Test in Young and Older Adults: Pattern of Gain and Impact of Educational Level. Exp Aging Res. 2020 Jan-Feb;46(1):52-67. doi: 10.1080/0361073X.2019.1693013
32. Brunet E, Sarfati Y, Hardy-Baylé MC. Reasoning about physical causality and other's intentions in schizophrenia. Cogn Neuropsychiatry 2003 May;8(2):129-39. doi: 10.1080/13546800244000256
33. Stone VE, Baron-Cohen S, Knight RT. Frontal lobe contributions to theory of mind. J Cogn Neurosci. 1998 Sep;10(5):640-56. doi: 10.1162/089892998562942
34. Boutantin J, Moroni C, Demeneix E, Marchand E, Lys H, Pasquier F, Delbeuck X. Normalisation du test des faux pas auprès d’une population adulte. 34es Journées de Printemps de la Société de Neuropsychologie de Langue Française. Lille 27-29 May, 2010.
35. Stroop JR. Studies of interference in serial verbal reactions. J Exp. Psychol. 1935;18(6):643–662. doi:10.1037/h0054651
36. Cardebat D, Doyon B, Puel M, Goulet P, Joanette Y. Formal and semantic lexical evocation in normal subjects. Performance and dynamics of production as a function of sex, age and educational level. Acta Neurol Belg. 1990;90(4):207-17.
37. 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. Cognitive deficits in Machado-Joseph disease correlate with hypoperfusion of visual system areas. Cerebellum 2012; 11(4):1037–44. doi:10.1007/s12311-012-0354-x
38. Wong CHY, Liu J, Lee TMC, Tao J, Wong AWK, Chau BKH, Chen L, Chan CCH. Fronto-cerebellar connectivity mediating cognitive processing speed. Neuroimage 2021 Feb 1;226:117556. doi: 10.1016/j.neuroimage.2020.117556