Social concepts and the cerebellum: behavioural and functional connectivity signatures in cerebellar ataxic patients.

cerebellar ataxia naturalistic texts resting-state functional connectivity social concepts voxel-based morphometry

Journal

Philosophical transactions of the Royal Society of London. Series B, Biological sciences
ISSN: 1471-2970
Titre abrégé: Philos Trans R Soc Lond B Biol Sci
Pays: England
ID NLM: 7503623

Informations de publication

Date de publication:
13 02 2023
Historique:
pmc-release: 13 02 2024
entrez: 26 12 2022
pubmed: 27 12 2022
medline: 28 12 2022
Statut: ppublish

Résumé

Neurocognitive research on social concepts underscores their reliance on fronto-temporo-limbic regions mediating broad socio-cognitive skills. Yet, the field has neglected another structure increasingly implicated in social cognition: the cerebellum. The present exploratory study examines this link combining a novel naturalistic text paradigm, a relevant atrophy model and functional magnetic resonance imaging. Fifteen cerebellar ataxia (CA) patients with focal cerebellar atrophy and 29 matched controls listened to a social text (highlighting interpersonal events) as well as a non-social text (focused on a single person's actions), and answered comprehension questionnaires. We compared behavioural outcomes between groups and examined their association with cerebellar connectivity. CA patients showed deficits in social text comprehension and normal scores in the non-social text. Also, social text outcomes in controls selectively correlated with connectivity between the cerebellum and key regions subserving multi-modal semantics and social cognition, including the superior and medial temporal gyri, the temporal pole and the insula. Conversely, brain-behaviour associations involving the cerebellum were abolished in the patients. Thus, cerebellar structures and connections seem involved in processing social concepts evoked by naturalistic discourse. Such findings invite new theoretical and translational developments integrating social neuroscience with embodied semantics. This article is part of the theme issue 'Concepts in interaction: social engagement and inner experiences'.

Identifiants

pubmed: 36571119
doi: 10.1098/rstb.2021.0364
pmc: PMC9791482
doi:

Banques de données

figshare
['10.6084/m9.figshare.c.6251596']

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

20210364

Subventions

Organisme : NIA NIH HHS
ID : R01 AG057234
Pays : United States

Références

Cereb Cortex. 2020 Oct 1;30(11):6051-6068
pubmed: 32577713
J Alzheimers Dis. 2017;55(4):1429-1435
pubmed: 27834777
Front Neurol. 2021 Mar 11;12:631722
pubmed: 33776890
Philos Trans R Soc Lond B Biol Sci. 2003 Mar 29;358(1431):459-73
pubmed: 12689373
Behav Neurol. 2010;23(1-2):17-29
pubmed: 20714058
Int J Neurosci. 2018 Feb;128(2):182-191
pubmed: 28877638
Front Hum Neurosci. 2014 Feb 14;8:60
pubmed: 24592227
Brain Lang. 2015 Feb;141:1-10
pubmed: 25498409
Cortex. 2020 Nov;132:460-472
pubmed: 32950239
Brain. 2009 Jun;132(Pt 6):1633-44
pubmed: 19451178
Annu Rev Neurosci. 2022 Jul 8;45:361-386
pubmed: 35385670
Cognition. 2018 Nov;180:135-157
pubmed: 30053570
Neurology. 2006 Jun 13;66(11):1717-20
pubmed: 16769946
Semin Neurol. 2002 Dec;22(4):375-84
pubmed: 12539058
Cerebellum. 2016 Dec;15(6):732-743
pubmed: 26585120
J Neurol Neurosurg Psychiatry. 2017 Sep;88(9):780-788
pubmed: 28501823
Prog Neuropsychopharmacol Biol Psychiatry. 2021 Aug 30;110:110328
pubmed: 33865925
Int J Dev Neurosci. 2005 Apr-May;23(2-3):125-41
pubmed: 15749240
Cerebellum. 2012 Mar;11(1):155-66
pubmed: 21701895
Mov Disord Clin Pract. 2019 Aug 16;6(7):531-540
pubmed: 31538086
Cereb Cortex. 2020 Apr 14;30(4):2157-2166
pubmed: 31665238
J Neurol. 2017 Jun;264(6):1118-1126
pubmed: 28478596
Proc Natl Acad Sci U S A. 2007 Apr 10;104(15):6430-5
pubmed: 17404215
J Neurosci. 2016 Apr 06;36(14):4050-5
pubmed: 27053211
Neurology. 2010 Feb 23;74(8):678-84
pubmed: 20177122
Sci Rep. 2019 Jul 31;9(1):11110
pubmed: 31366954
Proc Natl Acad Sci U S A. 2002 Nov 12;99(23):15238-43
pubmed: 12417766
Neuroimage. 2010 Jan 1;49(1):158-68
pubmed: 19631275
Nat Neurosci. 2017 Feb 23;20(3):299-303
pubmed: 28230846
Front Hum Neurosci. 2014 Feb 24;8:74
pubmed: 24605094
J Int Neuropsychol Soc. 2017 Feb;23(2):150-158
pubmed: 28205494
J Neurol. 2013 Dec;260(12):3134-43
pubmed: 24122064
Sci Rep. 2017 Oct 2;7(1):12538
pubmed: 28970538
World Psychiatry. 2006 Jun;5(2):77-81
pubmed: 16946939
Cortex. 2018 Mar;100:111-126
pubmed: 28764852
J Med Genet. 2017 Feb;54(2):114-124
pubmed: 27811304
Philos Trans R Soc Lond B Biol Sci. 2018 Aug 5;373(1752):
pubmed: 29915004
PLoS One. 2013 Oct 22;8(10):e77914
pubmed: 24167590
Front Neurosci. 2019 Nov 22;13:1259
pubmed: 31824254
Front Psychol. 2018 Jul 12;9:1194
pubmed: 30050490
Soc Cogn Affect Neurosci. 2012 Apr;7(4):467-75
pubmed: 21586527
J Alzheimers Dis. 2021;82(s1):S379-S394
pubmed: 33492297
Proc Natl Acad Sci U S A. 2005 May 24;102(21):7713-7
pubmed: 15897465
Nat Rev Neurosci. 2017 Feb;18(2):115-126
pubmed: 28053326
An Sist Sanit Navar. 2008 May-Aug;31(2):135-52
pubmed: 18953362
Cereb Cortex. 2022 Mar 07;:
pubmed: 35253864
J Alzheimers Dis. 2021;83(1):227-248
pubmed: 34275897
Cerebellum. 2019 Feb;18(1):147-151
pubmed: 29938355
Brain. 2016 Nov 1;139(11):3022-3040
pubmed: 27679483
Ann N Y Acad Sci. 2002 Dec;978:273-88
pubmed: 12582060
Cereb Cortex. 2018 Aug 1;28(8):2699-2710
pubmed: 28633369
Neuroimage. 2020 Aug 1;216:116820
pubmed: 32278096
J Int Adv Otol. 2019 Aug;15(2):304-308
pubmed: 31418719
Front Aging Neurosci. 2018 Oct 01;10:300
pubmed: 30327599
J Am Geriatr Soc. 2005 Apr;53(4):695-9
pubmed: 15817019
Trends Cogn Sci. 2012 Nov;16(11):559-72
pubmed: 23047070
Brain. 2017 Dec 1;140(12):3357-3377
pubmed: 29112719
J Neurosci. 2021 May 12;41(19):4276-4292
pubmed: 33827935
Front Psychol. 2018 Sep 19;9:1748
pubmed: 30283389
Behav Res Methods. 2005 Nov;37(4):665-71
pubmed: 16629300
Behav Cogn Neurosci Rev. 2006 Sep;5(3):107-27
pubmed: 16891554
Cerebellum. 2019 Oct;18(5):873-881
pubmed: 31422550
Cortex. 2021 May;138:101-112
pubmed: 33677324
Philos Trans R Soc Lond B Biol Sci. 2018 Aug 5;373(1752):
pubmed: 29915002
Cortex. 2021 Apr;137:93-107
pubmed: 33609899
Brain. 2022 Apr 29;145(3):1052-1068
pubmed: 34529034
Mov Disord. 2021 Feb;36(2):283-297
pubmed: 33022077
Hum Brain Mapp. 2015 Dec;36(12):5137-54
pubmed: 26419890
Neuropsychologia. 2016 Aug;89:217-224
pubmed: 27329686
Annu Rev Psychol. 2011;62:103-34
pubmed: 21126178
Neuroimage. 2021 Jul 15;235:117998
pubmed: 33789131
Cerebellum. 2020 Dec;19(6):833-868
pubmed: 32632709
J Neurosci. 2016 Jun 1;36(22):6002-10
pubmed: 27251621
Neuropsychologia. 1971 Mar;9(1):97-113
pubmed: 5146491
Soc Cogn Affect Neurosci. 2020 Jul 1;15(5):599-613
pubmed: 32507876
Trends Cogn Sci. 2013 Sep;17(9):458-70
pubmed: 23932069
Cortex. 2015 Aug;69:237-54
pubmed: 26103601
Neurol Clin Pract. 2016 Feb;6(1):61-68
pubmed: 26918204
Neuroimage. 2016 Jan 1;124(Pt A):248-255
pubmed: 26348560
J Int Neuropsychol Soc. 2009 Sep;15(5):777-86
pubmed: 19635178
Ann Clin Transl Neurol. 2016 Jun 21;3(8):572-87
pubmed: 27606341
Cereb Cortex. 2016 Jul;26(7):3205-18
pubmed: 26209844
Front Psychiatry. 2020 Nov 04;11:573002
pubmed: 33329111
Curr Top Behav Neurosci. 2017;30:379-396
pubmed: 27130326
Cereb Cortex. 2014 Jul;24(7):1767-77
pubmed: 23408565
Mov Disord. 2015 Sep;30(10):1391-9
pubmed: 26256273
Neuroimage. 2019 Aug 15;197:439-449
pubmed: 31059796
Cerebellum. 2015 Feb;14(1):35-8
pubmed: 25331541
Front Cell Neurosci. 2019 Jan 08;12:510
pubmed: 30670949
Neurology. 2012 Apr 24;78(17):1354-62
pubmed: 22529204
Cereb Cortex. 2022 Aug 3;32(16):3377-3391
pubmed: 34875690
Brain Imaging Behav. 2021 Aug;15(4):1912-1921
pubmed: 32897484
Adv Cogn Psychol. 2013 Mar 15;9(1):32-43
pubmed: 23853676

Auteurs

Pamela Lopes da Cunha (P)

Cognitive Neuroscience Center, University of San Andrés, Buenos Aires B1644BID, Argentina.
National Agency for Scientific Promotion and Technology (ANPCyT), Buenos Aires, C1425FQD, Argentina.

Sol Fittipaldi (S)

Cognitive Neuroscience Center, University of San Andrés, Buenos Aires B1644BID, Argentina.
National Scientific and Technical Research Council (CONICET), Buenos Aires, C1425FQB, Argentina.
Global Brain Health Institute, University of California San Francisco, 94158-2324, US and Trinity College Dublin, D02 PN40, Ireland.
Latin American Brain Health Institute (BrainLat), Adolfo Ibáñez University, Santiago, 7550344, Chile.

Cecilia González Campo (C)

Cognitive Neuroscience Center, University of San Andrés, Buenos Aires B1644BID, Argentina.
National Scientific and Technical Research Council (CONICET), Buenos Aires, C1425FQB, Argentina.

Marcelo Kauffman (M)

Consultorio y Laboratorio de Neurogenética, Centro Universitario de Neurología "José María Ramos Mejía" y División Neurología, Hospital JM Ramos Mejía, Facultad de Medicina, UBA, Buenos Aires, C1221ADC, Argentina.
School of Medicine, UBA, CONICET, Buenos Aires, C1121ABG, Argentina.

Sergio Rodríguez-Quiroga (S)

Consultorio y Laboratorio de Neurogenética, Centro Universitario de Neurología "José María Ramos Mejía" y División Neurología, Hospital JM Ramos Mejía, Facultad de Medicina, UBA, Buenos Aires, C1221ADC, Argentina.

Darío Andrés Yacovino (DA)

Department of Neurology, Dr. Cesar Milstein Hospital, Buenos Aires, C1221ACI, Argentina.
Memory and Balance Clinic, Buenos Aires, C1425BPC, Argentina.

Agustín Ibáñez (A)

Cognitive Neuroscience Center, University of San Andrés, Buenos Aires B1644BID, Argentina.
National Scientific and Technical Research Council (CONICET), Buenos Aires, C1425FQB, Argentina.
Global Brain Health Institute, University of California San Francisco, 94158-2324, US and Trinity College Dublin, D02 PN40, Ireland.
Latin American Brain Health Institute (BrainLat), Adolfo Ibáñez University, Santiago, 7550344, Chile.

Agustina Birba (A)

Cognitive Neuroscience Center, University of San Andrés, Buenos Aires B1644BID, Argentina.
National Scientific and Technical Research Council (CONICET), Buenos Aires, C1425FQB, Argentina.

Adolfo M García (AM)

Cognitive Neuroscience Center, University of San Andrés, Buenos Aires B1644BID, Argentina.
National Scientific and Technical Research Council (CONICET), Buenos Aires, C1425FQB, Argentina.
Global Brain Health Institute, University of California San Francisco, 94158-2324, US and Trinity College Dublin, D02 PN40, Ireland.
Departamento de Lingüística y Literatura, Facultad de Humanidades, Universidad de Santiago de Chile, Santiago, 9170022, Chile.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH