Slowness in Movement Initiation is Associated with Proactive Inhibitory Network Dysfunction in Parkinson’s Disease

Criaud, Marion; Poisson, Alice; Thobois, Stéphane; Météreau, Élise; Redouté, Jérôme; Ibarrola, Danièle; Baraduc, Pierre; Broussolle, Emmanuel; Strafella, Antonio P.; Ballanger, Bénédicte; Boulinguez, Philippe

doi:10.3233/jpd-150750

Cited by 21 publications

(29 citation statements)

References 51 publications

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“…Our results revealed abnormal proactive inhibition in the drug-treated patients and surgical patients with GPi-DBS off compared to the healthy controls. This is consistent with previous studies, which indicated proactive inhibition might be endogenously impaired in PD patients as a result of specific hypoactivation of a proactive inhibitory network ( Criaud et al, 2016 ). However, a mixed effect of medications and PD pathology would be a more reasonable interpretation of the results, as all the participants were using medication and robust evidence has confirmed the role of Parkinson’s medications in inhibitory control ( Voon et al, 2017 ).…”

Section: Discussionsupporting

confidence: 93%

Deep Brain Stimulation of the Internal Globus Pallidus Improves Response Initiation and Proactive Inhibition in Patients With Parkinson’s Disease

et al. 2018

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Background: Impulse control disorder is not uncommon in patients with Parkinson’s disease (PD) who are treated with dopamine replacement therapy and subthalamic deep brain stimulation (DBS). Internal globus pallidus (GPi)-DBS is increasingly used, but its role in inhibitory control has rarely been explored. In this study, we evaluated the effect of GPi-DBS on inhibitory control in PD patients.Methods: A stop-signal paradigm was used to test response initiation, proactive inhibition, and reactive inhibition. The subjects enrolled in the experiment were 27 patients with PD, of whom 13 had received only drug treatment and 14 had received bilateral GPi-DBS in addition to conventional medical treatment and 15 healthy individuals.Results: Our results revealed that with GPi-DBS on, patients with PD showed significantly faster responses than the other groups in trials where it was certain that no stop signal would be presented. Proactive inhibition was significantly different in the surgical patients with GPi-DBS on versus when GPi-DBS was off, in surgical patients with GPi-DBS on versus drug-treated patients, and in healthy controls versus drug-treated patients. Correlation analyses revealed that when GPi-DBS was on, there was a statistically significant moderate positive relationship between proactive inhibition and dopaminergic medication.Conclusion: GPi-DBS may lead to an increase in response initiation speed and improve the dysfunctional proactive inhibitory control observed in PD patients. Our results may help us to understand the role of the GPi in cortical-basal ganglia circuits.

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Section: Discussionsupporting

confidence: 93%

Deep Brain Stimulation of the Internal Globus Pallidus Improves Response Initiation and Proactive Inhibition in Patients With Parkinson’s Disease

et al. 2018

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“…) and related disorders in PD (Criaud et al . ). Second, these changes are observed in the critical alpha band, which indexes an active inhibitory mechanism relying on rhythmic local fluctuations of GABAergic inhibitory interneurons (Lőrincz et al .…”

Section: Discussionmentioning

confidence: 97%

“…; Criaud et al . ). This executive disorder concerns proactive inhibition, a function which is intended to inhibit movement triggering mechanisms in the absence of stimulation in uncertain environments.…”

mentioning

confidence: 97%

“…In accordance with this view, difficulties initiating movements are associated with pathological overactivity within the proactive inhibitory brain network (Criaud et al . ). Deep brain stimulation of the subthalamic nucleus would act by regaining control of the state of ‘self‐initiated automaticity’ (ibid).…”

mentioning

confidence: 97%

“…Conversely, Parkinson's disease patients show abnormally enhanced activity within the proactive inhibitory network leading to difficulties initiating movements (delayed responses, Criaud et al . ). As inferred from behavioral studies, the effect of STN‐DBS may consist in reinstating the ability to release proactive inhibitory control in the absence of stimulation when the context does not require action restraint (Favre et al .…”

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confidence: 97%

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Clonidine modulates the activity of the subthalamic‐supplementary motor loop: evidence from a pharmacological study combining deep brain stimulation and electroencephalography recordings in Parkinsonian patients

Spay

Albares

Lio

et al. 2018

Journal of Neurochemistry

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Clonidine is an anti-hypertensive medication which acts as an alpha-adrenergic receptor agonist. As the noradrenergic system is likely to support cognitive functions including attention and executive control, other clinical uses of clonidine have recently gained popularity for the treatment of neuropsychiatric disorders like attention-deficit hyperactivity disorder or Tourette syndrome, but the mechanism of action is still unclear. Here, we test the hypothesis that the noradrenergic system regulates the activity of subthalamo-motor cortical loops, and that this influence can be modulated by clonidine. We used pharmacological manipulation of clonidine in a placebo-controlled study in combination with subthalamic nucleus-deep brain stimulation (STN-DBS) in 16 Parkinson's disease patients performing a reaction time task requiring to refrain from reacting (proactive inhibition). We recorded electroencephalographical activity of the whole cortex, and applied spectral analyses directly at the source level after advanced blind source separation. We found only one cortical source localized to the supplementary motor area (SMA) that supported an interaction of pharmacological and subthalamic stimulation. Under placebo, STN-DBS reduced proactive alpha power in the SMA, a marker of local inhibitory activity. This effect was associated with the speeding-up of movement initiation. Clonidine substantially increased proactive alpha power from the SMA source, and canceled out the benefits of STN-DBS on movement initiation. These results provide the first direct neural evidence in humans that the tonic inhibitory activity of the subthalamocortical loops underlying the control of movement initiation is coupled to the noradrenergic system, and that this activity can be targeted by pharmacological agents acting on alpha-adrenergic receptors.

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Testing the physiological plausibility of conflicting psychological models of response inhibition: A forward inference fMRI study

Criaud¹,

Longcamp

Anton

et al. 2017

Behavioural Brain Research

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Slowness in Movement Initiation is Associated with Proactive Inhibitory Network Dysfunction in Parkinson’s Disease

Cited by 21 publications

References 51 publications

Deep Brain Stimulation of the Internal Globus Pallidus Improves Response Initiation and Proactive Inhibition in Patients With Parkinson’s Disease

Deep Brain Stimulation of the Internal Globus Pallidus Improves Response Initiation and Proactive Inhibition in Patients With Parkinson’s Disease

Clonidine modulates the activity of the subthalamic‐supplementary motor loop: evidence from a pharmacological study combining deep brain stimulation and electroencephalography recordings in Parkinsonian patients

Testing the physiological plausibility of conflicting psychological models of response inhibition: A forward inference fMRI study

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