Impulsivity in Parkinson’s disease is associated with altered subthalamic but not globus pallidus internus activity

Rossi, P. Justin; Shute, Jonathan; Opri, Enrico; Molina, Rene; Peden, Corinna; Castellanos, Oscar; Foote, Kelly D.; Gündüz, Ayşegül; Okun, Michael S.

doi:10.1136/jnnp-2016-315325

Cited by 17 publications

(10 citation statements)

References 16 publications

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“…This role of the STN is consistent with the involvement of the corticobasal ganglia circuits in proactive and reactive inhibition of movement and cognition 8,9 . Markers of impulse control disorders were found in the STN of PD patients during rest 10 and risk decision tasks 11,12 . However, a full understanding of the underlying activity at the single neuron level is still missing.…”

supporting

confidence: 67%

“…8,9 Markers of impulse control disorders were found in the STN of PD patients during rest 10 and risk decision tasks. 11,12 However, a full understanding of the underlying activity at the single neuron level is still missing. Here, we investigate the possibility of identifying subjects displaying ICB with microelectrode recordings (MERs) 13 performed at rest for target identification during DBS implant surgery.…”

mentioning

confidence: 99%

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Impulsivity Markers in Parkinsonian Subthalamic Single‐Unit Activity

Micheli

Vissani

Pecchioli³

et al. 2021

Movement Disorders

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Background: Impulsive-compulsive behaviors are common in Parkinson's disease (PD) patients. However, the basal ganglia dysfunctions associated with high impulsivity have not been fully characterized. The objective of this study was to identify the features associated with impulsive-compulsive behaviors in single neurons of the subthalamic nucleus (STN). Methods: We compared temporal and spectral features of 412 subthalamic neurons from 12 PD patients with impulsive-compulsive behaviors and 330 neurons from 12 PD patients without. Single-unit activities were extracted from exploratory microrecordings performed during deep brain stimulation (DBS) implant surgery in an OFF medication state. Results: Patients with impulsive-compulsive behaviors displayed decreased firing frequency during bursts and a larger fraction of tonic neurons combined with weaker beta coherence. Information carried by these features led to the identification of patients with impulsive-compulsive behaviors with an accuracy greater than 80%.

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supporting

confidence: 67%

mentioning

confidence: 99%

Impulsivity Markers in Parkinsonian Subthalamic Single‐Unit Activity

Micheli

Vissani

Pecchioli³

et al. 2021

Movement Disorders

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“…Several limitations in our study have to be addressed. The use of fictive monetary rewards may be considered a limitation, although it has been successfully used in previous similar experiments . Neuroimaging studies revealed that real and fictive rewards recruit overlapping neural networks, suggesting that our results could be reasonably extrapolated to a situation involving a real reward.…”

Section: Discussionmentioning

confidence: 82%

Effects of subthalamic nucleus stimulation and levodopa on decision‐making in Parkinson's disease

et al. 2019

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A BS TRACT: Background: Parkinson's disease (PD) is frequently associated with behavioral disorders, particularly within the spectrum of motivated behaviors such as apathy or impulsivity. Both pharmacological and neurosurgical treatments have an impact on these impairments. However, there still is controversy as to whether subthalamic nucleus deep brain stimulation (STN-DBS) can cause or reduce impulsive behaviors. Objectives: We aimed to identify the influence of functional surgery on decision-making processes in PD. Methods: We studied 13 PD patients and 13 healthy controls. The experimental task involved squeezing a dynamometer with variable force to obtain rewards of various values under four conditions: without treatment, with L-dopa or subthalamic stimulation alone, and with both L-dopa and subthalamic stimulation. Statistical analyses consisted of generalized linear mixed models including treatment condition, reward value, level of effort, and their interactions. We analyzed acceptance rate (the percentage of accepted trials), decision time, and force applied.Results: Comparatively to controls, patients without treatment exhibited lower acceptance rate and force applied. Patients under L-dopa alone did not exhibit increased acceptance rate. With subthalamic stimulation, either with or without added L-dopa, all measures were improved so that patients' behaviors were undistinguishable from healthy controls'. Conclusions: Our study shows that L-dopa administration does not fully restore cost-benefit decision-making processes, whereas STN-DBS fully normalizes patients' behaviors. These findings suggest that dopamine is partly involved in cost-benefit valuation, and that STN-DBS can have a beneficial effect on motivated behaviors in PD and may improve certain forms of impulsive behaviors.

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“…Few studies have examined the electrophysiology of PD patients with ICDs. PD patients with ICDs have proportionally more reward-responsive neurons and less loss-responsive neurons in the STN (159). In a stop signal task with a small sample of 10 PD patients, STN high frequency (35–75 Hz) oscillatory activity decreased during inhibition (160).…”

Section: Neural Substratementioning

confidence: 99%

Medications, Deep Brain Stimulation, and Other Factors Influencing Impulse Control Disorders in Parkinson's Disease

et al. 2019

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Impulse control disorders (ICDs) in Parkinson's disease (PD) have a high cumulative incidence and negatively impact quality of life. ICDs are influenced by a complex interaction of multiple factors. Although it is now well-recognized that dopaminergic treatments and especially dopamine agonists underpin many ICDs, medications alone are not the sole cause. Susceptibility to ICD is increased in the setting of PD. While causality can be challenging to ascertain, a wide range of modifiable and non-modifiable risk factors have been linked to ICDs. Common characteristics of PD patients with ICDs have been consistently identified across many studies; for example, males with an early age of PD onset and dopamine agonist use have a higher risk of ICD. However, not all cases of ICDs in PD can be directly attributable to dopamine, and studies have concluded that additional factors such as genetics, smoking, and/or depression may be more predictive. Beyond dopamine, other ICD associations have been described but remain difficult to explain, including deep brain stimulation surgery, especially in the setting of a reduction in dopaminergic medication use. In this review, we will summarize the demographic, genetic, behavioral, and clinical contributions potentially influencing ICD onset in PD. These associations may inspire future preventative or therapeutic strategies.

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Impulsivity in Parkinson’s disease is associated with altered subthalamic but not globus pallidus internus activity

Abstract: These findings provide further evidence of STN involvement in impulsive behaviour in the PD population.

Cited by 17 publications

References 16 publications

Impulsivity Markers in Parkinsonian Subthalamic Single‐Unit Activity

Impulsivity Markers in Parkinsonian Subthalamic Single‐Unit Activity

Effects of subthalamic nucleus stimulation and levodopa on decision‐making in Parkinson's disease

Medications, Deep Brain Stimulation, and Other Factors Influencing Impulse Control Disorders in Parkinson's Disease

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