Anterior lead location predicts verbal fluency decline following STN-DBS in Parkinson's disease

Greif, Taylor R.; Askari, Asra; Maher, Amanda Cook; Patil, Parag G.; Persad, Carol

doi:10.1016/j.parkreldis.2021.10.012

Cited by 12 publications

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References 27 publications

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“…[3][4][5] Findings from our previous work indicate that greater anterior displacement of the electrode from the left STN midpoint contributes to greater phonemic VF decline. 6 Recently, attention has also focused upon lesion-…”

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confidence: 99%

Decline of verbal fluency with lateral superior frontal gyrus penetration in subthalamic nucleus deep brain stimulation for Parkinson disease

Askari¹,

Greif

Lam³

et al. 2022

Journal of Neurosurgery

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OBJECTIVE Verbal fluency (VF) decline is a well-recognized adverse cognitive outcome following subthalamic nucleus deep brain stimulation (STN DBS) in patients with Parkinson disease (PD). The mechanisms underlying VF decline, whether from stimulation, lesioning, or both, remain unclear. This study aims to investigate the unique effects of DBS lead trajectory on VF beyond previously reported effects of active contact location. METHODS The study population included 56 patients with idiopathic PD who underwent bilateral STN DBS. Phonemic and semantic VF scores were compared pre- and postoperatively. Features of the electrode trajectory were measured on postoperative imaging, including distance from the falx cerebri, distance from the superior frontal sulcus, and caudate nucleus penetration. The authors used t-tests, Pearson’s correlation, and multiple linear regression analyses to examine the relationship between VF change and demographic, disease, and electrode trajectory variables. RESULTS The laterality of entry within the left superior frontal gyrus (SFG) predicted greater phonemic VF decline (sr2 = 0.28, p < 0.001) after controlling for active contact location. VF change did not differ by the presence of caudate nucleus penetration in either hemisphere (p > 0.05). CONCLUSIONS Lateral penetration of the SFG in the left hemisphere is associated with worsening phonemic VF and has greater explanatory power than active contact location. This may be explained by lesioning of the lateral SFG–Broca area pathway, which is implicated in language function.

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confidence: 99%

Decline of verbal fluency with lateral superior frontal gyrus penetration in subthalamic nucleus deep brain stimulation for Parkinson disease

Askari¹,

Greif

Lam³

et al. 2022

Journal of Neurosurgery

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“…Among various facets of cognitive function, declines in verbal fluency are the most common neuropsychological consequence of bilateral DBS for PD. 5,8,21,[37][38][39][40][41][42][43][44][45] While verbal fluency function typically deteriorates with PD progression, 46 declines following bilateral DBS are more pronounced than with best medical therapy alone. 8,13,44 Here we found hemisphere-effects on cognition following unilateral STN DBS.…”

Section: Discussionmentioning

confidence: 99%

“…Non‐motor function is relatively neglected in research on DBS and other stereotactic functional therapies. Among various facets of cognitive function, declines in verbal fluency are the most common neuropsychological consequence of bilateral DBS for PD 5,8,21,37–45 . While verbal fluency function typically deteriorates with PD progression, 46 declines following bilateral DBS are more pronounced than with best medical therapy alone 8,13,44 .…”

Section: Discussionmentioning

confidence: 99%

Differential Cognitive Effects of Unilateral Subthalamic Nucleus Deep Brain Stimulation for Parkinson's Disease

Del Bene,

Martin,

Brinkerhoff

et al. 2024

Annals of Neurology

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ObjectiveThe aim of this study was to investigate the cognitive effects of unilateral directional versus ring subthalamic nucleus deep brain stimulation (STN DBS) in patients with advanced Parkinson's disease.MethodsWe examined 31 participants who underwent unilateral STN DBS (left n = 17; right n = 14) as part of an National Institutes of Health (NIH)‐sponsored randomized, double‐blind, crossover study contrasting directional versus ring stimulation. All participants received unilateral DBS implants in the hemisphere more severely affected by motor parkinsonism. Measures of cognition included verbal fluency, auditory‐verbal memory, and response inhibition. We used mixed linear models to contrast the effects of directional versus ring stimulation and implant hemisphere on longitudinal cognitive function.ResultsCrossover analyses showed no evidence for group‐level changes in cognitive performance related to directional versus ring stimulation. Implant hemisphere, however, impacted cognition in several ways. Left STN participants had lower baseline verbal fluency than patients with right implants (t [20.66 = −2.50, p = 0.02]). Verbal fluency declined after left (p = 0.013) but increased after right STN DBS (p < 0.001), and response inhibition was faster following right STN DBS (p = 0.031). Regardless of hemisphere, delayed recall declined modestly over time versus baseline (p = 0.001), and immediate recall was unchanged.InterpretationDirectional versus ring STN DBS did not differentially affect cognition. Similar to prior bilateral DBS studies, unilateral left stimulation worsened verbal fluency performance. In contrast, unilateral right STN surgery increased performance on verbal fluency and response inhibition tasks. Our findings raise the hypothesis that unilateral right STN DBS in selected patients with predominant right brain motor parkinsonism could mitigate declines in verbal fluency associated with the bilateral intervention. ANN NEUROL 2024

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“…Another study found an association between trajectory angle and verbal fluency declines. Specifically, a lateral point of entry through the left superior frontal gyrus was associated with higher levels of verbal fluency decline from baseline, with no change in verbal fluency observed when the approach is through the caudate nucleus 54 , although others have shown that caudate penetration is associated with increased risk of decline in global cognition and working memory 18 It is likely that the microlesion effect in the left hemisphere disrupts the basal-ganglia-thalamocortical network, yielding verbal fluency declines, which may potentially be exacerbated by the stimulator depending on the DBS lead location 41,55 . A similar mechanism may explain the mild declines in auditory-verbal memory retrieval seen in our sample 56 .…”

Section: Discussionmentioning

confidence: 99%

Differential cognitive effects of unilateral left and right subthalamic nucleus deep brain stimulation for Parkinson disease

Bene

Martin

Brinkerhoff

et al. 2023

Preprint

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ObjectiveTo investigate hemispheric effects of directional versus ring subthalamic nucleus (STN) deep brain stimulation (DBS) surgery on cognitive function in patients with advanced Parkinson’s disease (PD).MethodsWe examined 31 PD patients (Left STN n = 17; Right STN n = 14) who underwent unilateral subthalamic nucleus (STN) DBS as part of a NIH-sponsored randomized, cross-over, double-blind (ring vs directional) clinical trial. Outcome measures were tests of verbal fluency, auditory-verbal memory, and response inhibition. First, all participants were pooled together to study the effects of directional versus ring stimulation. Then, we stratified the groups by surgery hemisphere and studied the longitudinal changes in cognition post-unilateral STN DBS.ResultsRelative to pre-DBS cognitive baseline performances, there were no group changes in cognition following unilateral DBS for either directional or ring stimulation. However, assessment of unilateral DBS by hemisphere revealed a different pattern. The left STN DBS group had lower verbal fluency than the right STN group (t(20.66 = -2.50,p= 0.02). Over a period of eight months post-DBS, verbal fluency declined in the left STN DBS group (p= 0.013) and improved in the right STN DBS group over time (p< .001). Similarly, response inhibition improved following right STN DBS (p= 0.031). Immediate recall did not significantly differ over time, nor was it affected by implant hemisphere, but delayed recall equivalently declined over time for both left and right STN DBS groups (left STN DBSp= 0.001, right STN DBS differ from left STN DBSp= 0.794).ConclusionsDirectional and ring DBS did not differentially or adversely affect cognition over time. Regarding hemisphere effects, verbal fluency decline was observed in those who received left STN DBS, along with the left and right STN DBS declines in delayed memory. The left STN DBS verbal fluency decrement is consistent with prior bilateral DBS research, likely reflecting disruption of the basal-ganglia-thalamocortical network connecting STN and inferior frontal gyrus. Interestingly, we found an improvement in verbal fluency and response inhibition following right STN DBS. It is possible that unilateral STN DBS, particularly in the right hemisphere, may mitigate cognitive decline.

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Anterior lead location predicts verbal fluency decline following STN-DBS in Parkinson's disease

Cited by 12 publications

References 27 publications

Decline of verbal fluency with lateral superior frontal gyrus penetration in subthalamic nucleus deep brain stimulation for Parkinson disease

Decline of verbal fluency with lateral superior frontal gyrus penetration in subthalamic nucleus deep brain stimulation for Parkinson disease

Differential Cognitive Effects of Unilateral Subthalamic Nucleus Deep Brain Stimulation for Parkinson's Disease

Differential cognitive effects of unilateral left and right subthalamic nucleus deep brain stimulation for Parkinson disease

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