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July 12, 2022; 99 (2) Research Article

Impulsivity Trait Profiles in Patients With Cerebellar Ataxia and Parkinson Disease

Tiffany X. Chen, Chi-Ying R. Lin, Megan A. Aumann, Yan Yan, Nadia Amokrane, Natasha A. Desai, Hakmook Kang, Daniel O. Claassen, View ORCID ProfileSheng-Han Kuo
First published April 15, 2022, DOI: https://doi.org/10.1212/WNL.0000000000200349
Tiffany X. Chen
From the Department of Neurology (T.X.C., N.A., N.A.D., S.-H.K.) and Initiative of Columbia Ataxia and Tremor (T.X.C., N.A., N.A.D., S.-H.K.), Columbia University Medical Center, New York, NY; Department of Biomedical Engineering (T.X.C.), Johns Hopkins University, Baltimore, MD; Department of Neurology (C.-Y.R.L.), Baylor College of Medicine, Houston, TX; Vanderbilt Brain Institute (M.A.A.), Department of Psychology, Vanderbilt University; and Departments of Neurology (M.A.A., D.O.C.) and Statistics (Y.Y., H.K.), Vanderbilt University Medical Center, Nashville, TN.
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Chi-Ying R. Lin
From the Department of Neurology (T.X.C., N.A., N.A.D., S.-H.K.) and Initiative of Columbia Ataxia and Tremor (T.X.C., N.A., N.A.D., S.-H.K.), Columbia University Medical Center, New York, NY; Department of Biomedical Engineering (T.X.C.), Johns Hopkins University, Baltimore, MD; Department of Neurology (C.-Y.R.L.), Baylor College of Medicine, Houston, TX; Vanderbilt Brain Institute (M.A.A.), Department of Psychology, Vanderbilt University; and Departments of Neurology (M.A.A., D.O.C.) and Statistics (Y.Y., H.K.), Vanderbilt University Medical Center, Nashville, TN.
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Megan A. Aumann
From the Department of Neurology (T.X.C., N.A., N.A.D., S.-H.K.) and Initiative of Columbia Ataxia and Tremor (T.X.C., N.A., N.A.D., S.-H.K.), Columbia University Medical Center, New York, NY; Department of Biomedical Engineering (T.X.C.), Johns Hopkins University, Baltimore, MD; Department of Neurology (C.-Y.R.L.), Baylor College of Medicine, Houston, TX; Vanderbilt Brain Institute (M.A.A.), Department of Psychology, Vanderbilt University; and Departments of Neurology (M.A.A., D.O.C.) and Statistics (Y.Y., H.K.), Vanderbilt University Medical Center, Nashville, TN.
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Yan Yan
From the Department of Neurology (T.X.C., N.A., N.A.D., S.-H.K.) and Initiative of Columbia Ataxia and Tremor (T.X.C., N.A., N.A.D., S.-H.K.), Columbia University Medical Center, New York, NY; Department of Biomedical Engineering (T.X.C.), Johns Hopkins University, Baltimore, MD; Department of Neurology (C.-Y.R.L.), Baylor College of Medicine, Houston, TX; Vanderbilt Brain Institute (M.A.A.), Department of Psychology, Vanderbilt University; and Departments of Neurology (M.A.A., D.O.C.) and Statistics (Y.Y., H.K.), Vanderbilt University Medical Center, Nashville, TN.
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Nadia Amokrane
From the Department of Neurology (T.X.C., N.A., N.A.D., S.-H.K.) and Initiative of Columbia Ataxia and Tremor (T.X.C., N.A., N.A.D., S.-H.K.), Columbia University Medical Center, New York, NY; Department of Biomedical Engineering (T.X.C.), Johns Hopkins University, Baltimore, MD; Department of Neurology (C.-Y.R.L.), Baylor College of Medicine, Houston, TX; Vanderbilt Brain Institute (M.A.A.), Department of Psychology, Vanderbilt University; and Departments of Neurology (M.A.A., D.O.C.) and Statistics (Y.Y., H.K.), Vanderbilt University Medical Center, Nashville, TN.
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Natasha A. Desai
From the Department of Neurology (T.X.C., N.A., N.A.D., S.-H.K.) and Initiative of Columbia Ataxia and Tremor (T.X.C., N.A., N.A.D., S.-H.K.), Columbia University Medical Center, New York, NY; Department of Biomedical Engineering (T.X.C.), Johns Hopkins University, Baltimore, MD; Department of Neurology (C.-Y.R.L.), Baylor College of Medicine, Houston, TX; Vanderbilt Brain Institute (M.A.A.), Department of Psychology, Vanderbilt University; and Departments of Neurology (M.A.A., D.O.C.) and Statistics (Y.Y., H.K.), Vanderbilt University Medical Center, Nashville, TN.
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Hakmook Kang
From the Department of Neurology (T.X.C., N.A., N.A.D., S.-H.K.) and Initiative of Columbia Ataxia and Tremor (T.X.C., N.A., N.A.D., S.-H.K.), Columbia University Medical Center, New York, NY; Department of Biomedical Engineering (T.X.C.), Johns Hopkins University, Baltimore, MD; Department of Neurology (C.-Y.R.L.), Baylor College of Medicine, Houston, TX; Vanderbilt Brain Institute (M.A.A.), Department of Psychology, Vanderbilt University; and Departments of Neurology (M.A.A., D.O.C.) and Statistics (Y.Y., H.K.), Vanderbilt University Medical Center, Nashville, TN.
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Daniel O. Claassen
From the Department of Neurology (T.X.C., N.A., N.A.D., S.-H.K.) and Initiative of Columbia Ataxia and Tremor (T.X.C., N.A., N.A.D., S.-H.K.), Columbia University Medical Center, New York, NY; Department of Biomedical Engineering (T.X.C.), Johns Hopkins University, Baltimore, MD; Department of Neurology (C.-Y.R.L.), Baylor College of Medicine, Houston, TX; Vanderbilt Brain Institute (M.A.A.), Department of Psychology, Vanderbilt University; and Departments of Neurology (M.A.A., D.O.C.) and Statistics (Y.Y., H.K.), Vanderbilt University Medical Center, Nashville, TN.
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Sheng-Han Kuo
From the Department of Neurology (T.X.C., N.A., N.A.D., S.-H.K.) and Initiative of Columbia Ataxia and Tremor (T.X.C., N.A., N.A.D., S.-H.K.), Columbia University Medical Center, New York, NY; Department of Biomedical Engineering (T.X.C.), Johns Hopkins University, Baltimore, MD; Department of Neurology (C.-Y.R.L.), Baylor College of Medicine, Houston, TX; Vanderbilt Brain Institute (M.A.A.), Department of Psychology, Vanderbilt University; and Departments of Neurology (M.A.A., D.O.C.) and Statistics (Y.Y., H.K.), Vanderbilt University Medical Center, Nashville, TN.
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  • ORCID record for Sheng-Han Kuo
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Impulsivity Trait Profiles in Patients With Cerebellar Ataxia and Parkinson Disease
Tiffany X. Chen, Chi-Ying R. Lin, Megan A. Aumann, Yan Yan, Nadia Amokrane, Natasha A. Desai, Hakmook Kang, Daniel O. Claassen, Sheng-Han Kuo
Neurology Jul 2022, 99 (2) e176-e186; DOI: 10.1212/WNL.0000000000200349

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  • Impulsivity Trait Profiles in Patients With Cerebellar Ataxia and Parkinson Disease - January 31, 2023
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Abstract

Background and Objectives Individuals with cerebellar ataxia (CA) can develop impulsive behavioral symptoms, often resulting in negative interpersonal consequences, detrimentally affecting their quality of life. Limited evidence exists concerning impulsivity in CA and its associated behavioral changes. We assessed impulsive traits in CA using the Barratt Impulsivity Scale (BIS-11) and compared them with those of Parkinson disease (PD) to investigate the differences in the impulsive trait profiles between CA and PD.

Methods We conducted a dual-center cross-sectional study with individuals with CA and PD enrolled through consecutive sampling from movement disorders clinics at Columbia University Medical Center and Vanderbilt University Medical Center, respectively. Age-matched controls were recruited at the respective institutions. Participants were excluded if they had prior or comorbid neurologic and psychiatric diseases known to be associated with impulsivity. All participants completed the BIS-11 questionnaire as a measure of impulsive traits. We used a general linear model and a least absolute shrinkage and selection operation regression to compare the total, subscale, and individual items of the BIS-11 scores between groups. Subgroup analyses were performed to isolate cerebellar contributions to impulsivity from potential effects of extracerebellar pathology and dopaminergic dysfunction or medications.

Results A total of 190 participants—90 age-matched controls, 50 participants with CA, and 50 with PD—completed the assessments. Persons with CA reported 9.7% higher BIS-11 scores than controls (p < 0.001), while persons with PD reported 24.9% higher scores than controls (p < 0.001). In CA, the most affected domain of impulsivity was nonplanning. In contrast, persons with PD noted greater impulsivity across the nonplanning, attentional, and motor domains.

Discussion Impulsivity in CA is uniquely driven by the nonplanning trait, unlike in PD. This suggests that the cerebellum and basal ganglia may differentially govern impulsive behaviors with the cerebellum contributing to the brain circuitry of impulsivity in a domain-specific manner.

Glossary

BIS-11=
Barratt Impulsivity Scale;
CA=
cerebellar ataxia;
CCAS=
cerebellar cognitive affective syndrome;
FA=
Friedrich ataxia;
FDR=
false discovery rate;
GLM=
generalized linear model;
ILOCA=
idiopathic late-onset CA;
LASSO=
least absolute shrinkage and selection operation;
MSA-C=
multiple system atrophy–cerebellar type;
PD=
Parkinson disease;
SCA=
spinocerebellar ataxia

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Submitted and externally peer reviewed. The handling editors were José Merino, MD, PHIL, FAAN, and Peter Hedera, MD, PhD.

  • Received November 24, 2021.
  • Accepted in final form February 21, 2022.
  • © 2022 American Academy of Neurology
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