Impulsivity in Cerebellar Ataxias: Testing the Cerebellar Reward Hypothesis in Humans

Amokrane, Nadia; Viswanathan, Anisha; Freedman, Samantha N.; Yang, Ching-Ping; Desai, Natasha; Pan, Ming‐Kai; Kuo, Sheng‐Han; Lin, Chi‐Ying

doi:10.1002/mds.28121

Cited by 14 publications

(9 citation statements)

References 7 publications

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“…The classical symptoms related to abnormal reward processing in humans are impulsivity and compulsivity, 22 which can have tremendous impacts on individuals' lives. 23 , 24 , 25 Consistent with animal studies, 12 we recently found that people with cerebellar ataxia have increased impulse control behaviors (ICBs), including but not limited to excessive video game playing, binge eating, and hoarding, 23 , 24 further supporting the hypothesis that an intact cerebellum is crucial for reward processing in humans. These clinical observations further strengthen the new role of the cerebellum in reward processing actually occurs in humans.…”

Section: Introductionsupporting

confidence: 69%

Cerebellar impulsivity–compulsivity assessment scale

Lin

Amokrane

Chen

et al. 2022

Ann Clin Transl Neurol

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Objective The cerebellum has been identified as the key brain region that modulates reward processing in animal models. Consistently, we recently found that people with cerebellar ataxia have impulsive and compulsive behaviors (ICBs), the main symptoms related to abnormal reward processing. Due to the lack of a validated scale to quantitatively measure ICBs in cerebellar disorders, we aim to develop and validate a new scale, Cerebellar Impulsivity–Compulsivity Assessment (CIA). Methods We recruited 62 cerebellar ataxia cases, categorized into those with ICBs and those without. We developed a preliminary version of CIA, containing 17 questions. We studied the internal consistency, test–retest reliability, and inter‐rater reliability to formulate the final version of CIA, which constitutes only 10 questions. The receiver operating characteristic curve (ROC) was generated to assess the sensitivity and specificity of CIA. Results Cerebellar ataxia cases with ICBs have threefold higher total preliminary CIA scores than those without ICBs (12.06 ± 5.96 vs. 4.68 ± 3.50, p = 0.038 ). Cronbach's alpha revealed good internal consistency across all items ( α > 0.70 ). By performing the test–retest reliability and inter‐rater reliability on the preliminary version of CIA, we excluded seven questions ( r < 0.70) and generated the final version of CIA. Based on the ROC, a score of 8.0 in CIA was chosen as the cut‐off for ICBs in individuals with cerebellar ataxia with 81% sensitivity and 81% specificity. Interpretation CIA is a novel tool to assess ICBs in cerebellar ataxia and broaden our understanding of the cerebellum‐related cognitive and behavioral symptoms.

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Section: Introductionsupporting

confidence: 69%

Cerebellar impulsivity–compulsivity assessment scale

Lin

Amokrane

Chen

et al. 2022

Ann Clin Transl Neurol

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“…9 These findings are supported by our recent clinical observations of heightened impulsivity in patients with CA; specifically, the associated behavioral changes include increased gambling, hobbyism and punding, and medication overuse. 10,11 However, these impulsive behaviors can originate from distinct combinations of underlying traits. 5,24 With the use of a multitrait model of impulsivity, the results of our present study indicate that impulsivity in CA arises specifically as a result of disordered planning from a lack of cognitive complexity, which differs from the profile of impulsive traits seen in PD.…”

Section: Discussionmentioning

confidence: 99%

“…9 Consistent with these preclinical findings, we independently identified that patients with cerebellar ataxia (CA) can often engage in impulsive behaviors. 10,11 However, different sets of impulsive personality traits can drive a particular impulsive action. For example, a person may impulsively engage in gambling due to an inability to inhibit reward-based motivations (i.e., motor impulsivity) or an inability to consider the negative consequences of losing money (i.e., nonplanning impulsivity).…”

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confidence: 99%

Impulsivity Trait Profiles in Patients With Cerebellar Ataxia and Parkinson Disease

et al. 2022

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Background and Objectives:Individuals with cerebellar ataxia (CA) can develop impulsive behavioral symptoms, often resulting in negative interpersonal consequences, detrimentally impacting 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), in order to investigate the differences in the impulsive trait profiles between CA and PD.Methods:We conducted a dual-center cross-sectional study with CA and PD subjects 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 neurological and psychiatric diseases known to be associated with impulsivity. All subjects 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 CA, and 50 PD participants completed the assessments. Persons with CA reported 9.7% greater BIS-11 scores than controls (p < 0.001), while persons with PD participants reported 24.9% higher than controls (p < 0.001). In CA, the most impacted domain of impulsivity was non-planning. In contrast, persons with PD noted greater impulsivity across the non-planning, attentional, and motor domains.Discussion:Impulsivity in CA is uniquely driven by the non-planning 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.

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“…52,53 In particular, recent findings have indicated that individuals with CA have heightened domain-specific impulsive and compulsive behaviors, which is a common symptom of underlying reward system dysfunction. 54,55 Our study adds to this work by suggesting that the cerebellum is additionally necessary for reward learning in humans.…”

Section: Discussionmentioning

confidence: 59%

The role of the cerebellum in learning to predict reward: evidence from cerebellar ataxia

Nicholas

Amlang

Lin

et al. 2022

Preprint

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Recent findings in animals have challenged the traditional view of the cerebellum solely as the site of motor control, suggesting that the cerebellum may also be important for learning to predict reward from trial-and-error feedback. Yet, evidence for the role of the cerebellum in reward learning in humans is lacking. Moreover, open questions remain about which specific aspects of reward learning the cerebellum may contribute to. Here we address this gap through an investigation of multiple forms of reward learning in individuals with cerebellum dysfunction, represented by cerebellar ataxia cases. Nineteen participants with cerebellar ataxia and 57 age- and sex-matched healthy controls completed two separate tasks that required learning about reward contingencies from trial-and-error. To probe the selectivity of reward learning processes, the tasks differed in their underlying structure: while one task measured incremental reward learning ability alone, the other allowed participants to use an alternative learning strategy based on episodic memory alongside incremental reward learning. We found that individuals with cerebellar ataxia were profoundly impaired at reward learning from trial-and-error feedback on both tasks, but retained the ability to learn to predict reward based on episodic memory. These findings provide evidence from humans for a specific and necessary role for the cerebellum in incremental learning of reward associations based on reinforcement. More broadly, the findings suggest that alongside its role in motor learning, the cerebellum likely operates in concert with the basal ganglia to support reinforcement learning from reward.

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Impulsivity in Cerebellar Ataxias: Testing the Cerebellar Reward Hypothesis in Humans

Cited by 14 publications

References 7 publications

Cerebellar impulsivity–compulsivity assessment scale

Cerebellar impulsivity–compulsivity assessment scale

Impulsivity Trait Profiles in Patients With Cerebellar Ataxia and Parkinson Disease

The role of the cerebellum in learning to predict reward: evidence from cerebellar ataxia

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