The effects of unilateral versus bilateral subthalamic nucleus deep brain stimulation on prosaccades and antisaccades in Parkinson’s disease

Goelz, Lisa C.; David, Fabian J.; Sweeney, John A.; Vaillancourt, David E.; Poizner, Howard; Metman, Leonard Verhagen; Corcos, Daniel M.

doi:10.1007/s00221-016-4830-2

Cited by 28 publications

(53 citation statements)

References 57 publications

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“…Previous attempts at examining the effect of STN DBS on anti-saccade behavior have produced variable observations. Of several studies that specifically addresses effects of STN DBS of anti-saccades [28][29][30] , only one evaluated patients in their off-L-dopa condition, reporting results similar to the present study 30 . Two other studies 28,29 tested patients while they were on their regular dose of L-dopa, and reported no significant effect of STN DBS on anti-saccade performance.…”

Section: Discussionsupporting

confidence: 73%

The Role of the Subthalamic Nucleus in Inhibitory Control of Oculomotor Behavior in Parkinson’s Disease

Bakhtiari

Altınkaya

Pack

et al. 2020

Sci Rep

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, christopher c. pack & Abbas f. Sadikot * inhibiting inappropriate actions in a context is an important part of the human cognitive repertoire, and deficiencies in this ability are common in neurological and psychiatric disorders. An anti-saccade is a simple oculomotor task that tests this ability by requiring inhibition of saccades to peripheral targets (pro-saccade) and producing voluntary eye movements toward the mirror position (anti-saccades). Previous studies provide evidence for a possible contribution from the basal ganglia in anti-saccade behavior, but the precise role of different components is still unclear. Parkinson's disease patients with implanted deep brain stimulators (DBS) in subthalamic nucleus (STN) provide a unique opportunity to investigate the role of the STN in anti-saccade behavior. Previous attempts to show the effect of STN DBS on anti-saccades have produced conflicting observations. For example, the effect of STN DBS on anti-saccade error rate is not yet clear. Part of this inconsistency may be related to differences in dopaminergic states in different studies. Here, we tested Parkinson's disease patients on anti-and pro-saccade tasks ON and OFF STN DBS, in ON and OFF dopaminergic medication states. First, STN DBS increases anti-saccade error rate while patients are OFF dopamine replacement therapy. Second, dopamine replacement therapy and STN DBS interact: L-dopa reduces the effect of STN DBS on antisaccade error rate. Third, STN DBS induces different effects on pro-and anti-saccades in different patients. these observations provide evidence for an important role for the Stn in the circuitry underlying context-dependent modulation of visuomotor action selection. Neuromodulation or Deep Brain Stimulation (DBS) of several subcortical areas significantly improves motor function in Parkinson's disease (PD) 1,2. Stimulation of the subthalamic nucleus (STN) improves tremor, drug-induced dyskinesias and motor fluctuations, and may also modulate aspects of executive cognition or emotion 3-6. However, unlike its motor outcome, the effect of subthalamic DBS on higher order executive functions remains uncertain. An important component of executive function is inhibitory control: the ability to suppress an impulsive response to external events due to an inappropriate context 7. Dysfunction of inhibitory control is involved in several psychiatric conditions, such as mood disorders, disorders of thought, and addiction 8,9. In PD, a deficiency of inhibitory control has been reported in different experimental tasks, such as the stop signal task 10 , and the Stroop task 11 , and impulse control may be worsened by therapies in some patients 12,13. Eye movements can be measured precisely and objectively (with 1 ms temporal resolution and approximately 0.5 degree spatial resolution) by using state-of-the-art eye-tracking technologies. This advance has made eye movements a popular readout behavior for probing different aspects of cognition with potential applications in clinical assessments 14. One well-...

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Section: Discussionsupporting

confidence: 73%

The Role of the Subthalamic Nucleus in Inhibitory Control of Oculomotor Behavior in Parkinson’s Disease

Bakhtiari

Altınkaya

Pack

et al. 2020

Sci Rep

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“…The dorsolateral prefrontal cortex has been shown to be active during coordinative tasks that involve spatial working memory (Barbey et al 2013; Owen et al 2005), and basal ganglia-prefrontal and basal ganglia-fronto-parietal networks have been shown to be active during the initiation phase of motor sequences (Boecker et al 2008). Interestingly, it has been shown that bilateral, but not unilateral, STN DBS can impair coordinative aspects of movement, for instance performance on a cognitive-motor dual-task (Alberts et al 2008), and response inhibition on the antisaccade task (Goelz et al 2017). Importantly, the cognitive task (n-back) implemented in the Alberts’ study and the antisaccade task implemented in the Goelz’ study both rely heavily upon prefrontal cortical areas (Alberts et al 2008; Goelz et al 2017).…”

Section: Introductionmentioning

confidence: 99%

Bilateral deep brain stimulation of the subthalamic nucleus increases pointing error during memory-guided sequential reaching

et al. 2018

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Deep brain stimulation of the subthalamic nucleus (STN DBS) significantly improves clinical motor symptoms, as well as intensive aspects of movement like velocity and amplitude in patients with Parkinson's disease (PD). However, the effects of bilateral STN DBS on integrative and coordinative aspects of motor control are equivocal. The aim of this study was to investigate the effects of bilateral STN DBS on integrative and coordinative aspects of movement using a memory-guided sequential reaching task. The primary outcomes were eye and finger velocity and end-point error. We expected that bilateral STN DBS would increase reaching velocity. More importantly, we hypothesized that bilateral STN DBS would increase eye and finger end-point error and this would not simply be the result of a speed accuracy trade-off. Ten patients with PD and bilaterally implanted subthalamic stimulators performed a memory-guided sequential reaching task under four stimulator conditions (DBS-OFF, DBS-LEFT, DBS-RIGHT, and DBS-BILATERAL) over 4 days. DBS-BILATERAL significantly increased eye velocity compared to DBS-OFF, DBS-LEFT, and DBS-RIGHT. It also increased finger velocity compared to DBS-OFF and DBS-RIGHT. DBS-BILATERAL did not change eye end-point error. The novel finding was that DBS-BILATERAL increased finger end-point error compared to DBS-OFF, DBS-LEFT, and DBS-RIGHT even after adjusting for differences in velocity. We conclude that bilateral STN DBS may facilitate basal ganglia-cortical networks that underlie intensive aspects of movement like velocity, but it may disrupt selective basal ganglia-cortical networks that underlie certain integrative and coordinative aspects of movement such as spatial accuracy.

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“…Thus, it is admitted that bilateral STN-DBS induces greater therapeutic effect (2). However, bilateral STN-DBS seems also to induce more deleterious side effects, aggravating cognitive processes, verbal fluidity and weight gain in a greater proportion than unilateral stimulation (35,38,39). We previously made the unique description of post-STN-DBS apathy in bilaterally stimulated patients, that was not correlated to dopaminergic reduction (Figure 3)(15-17, 31).…”

Section: Clinical Studymentioning

confidence: 97%

“…Bilateral STN-DBS is applied in patients suffering from advanced stage PD or/with symmetrical symptoms whereas unilateral STN-DBS is advocated for asymmetrical and/or mild stage PD (2). Few clinical studies compared unilateral and bilateral STN-DBS in same patients, but consistently, they highlight that bilateral STN-DBS seems more effective to alleviate motor disturbances such as gait, shaking and oculomotor control (35)(36)(37)41). Thus, it is admitted that bilateral STN-DBS induces greater therapeutic effect (2).…”

Section: Clinical Studymentioning

confidence: 99%

“…Although we demonstrated the deleterious effect of STN-DBS applied bilaterally, those of unilateral STN-DBS remains to be investigated either in the clinic or in preclinical approaches. Bilateral STN-DBS permits strongest motor improvements (35)(36)(37), but might also induce more non motor sides-effects than unilateral STN-DBS (35,38,39). Thus, one can hypothesize that unilateral STN-DBS effects on apathy could be weaker.…”

Section: Introductionmentioning

confidence: 99%

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Unilateral and Bilateral Subthalamic stimulation differently promote apathy: a translational approach

Vachez

Bahout

Magnard

et al. 2020

Preprint

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Apathy is frequently reported in Parkinson's disease (PD) patients under subthalamic nucleus deep brain stimulation (STN-DBS). The prevailing clinical view for apathy following STN-DBS is the reduction of dopaminergic medication. However, few clinical reports and recent experimental data suggested the pathogenicity of bilateral STN-DBS on motivation, challenging the leading opinion. Here, we investigate whether bilateralism of STN-DBS influences apathy outcome after STN-DBS, combining pre-clinical and clinical approaches. We assess the motivational effects of chronic unilateral STN-DBS in rats in the exact same conditions having highlighted a loss of motivation under bilateral STN-DBS. Clinical data are obtained by the follow-up of a cohort of parkinsonian patients undergoing unilateral STN-DBS and coming from the clinical center that described apathy related to bilateral STN-DBS itself.Despite an acute effect, which fades rapidly, unilateral STN-DBS did not induce a loss of motivation reminiscent to apathy in rats. In patients, apathy did not increase between the preoperative and the post-operative assessment. Together, those data demonstrate that bilateral but not unilateral STN-DBS can induce a loss of motivation in both rats and patients.This constitutes another evidence of the role of STN-DBS itself for apathy in PD.

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The effects of unilateral versus bilateral subthalamic nucleus deep brain stimulation on prosaccades and antisaccades in Parkinson’s disease

Cited by 28 publications

References 57 publications

The Role of the Subthalamic Nucleus in Inhibitory Control of Oculomotor Behavior in Parkinson’s Disease

The Role of the Subthalamic Nucleus in Inhibitory Control of Oculomotor Behavior in Parkinson’s Disease

Bilateral deep brain stimulation of the subthalamic nucleus increases pointing error during memory-guided sequential reaching

Unilateral and Bilateral Subthalamic stimulation differently promote apathy: a translational approach

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