Combining Multimodal Biomarkers to Guide Deep Brain Stimulation Programming in Parkinson Disease

Shah, Ashesh; Nguyen, T. A. Khoa; Peterman, Katrin; Khawaldeh, Saed; Debove, Ines; Shah, Syed Ahmar; Torrecillos, Flavie; Tan, Huiling; Pogosyan, Alek; Lachenmayer, M. Lenard; Michelis, Joan Philipp; Brown, Peter; Pollo, Claudio; Krack, Paul; Nowacki, Andreas; Tinkhauser, Gerd

doi:10.1016/j.neurom.2022.01.017

Cited by 27 publications

(37 citation statements)

References 47 publications

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“…The utility of an LFP-based approach to guide DBS programming is supported by a recent study combining multiple LFP spectral features to inform the selection of stimulation contact in PD (Shah et al, 2022 ). Compared with using β -range oscillations as the single feature, adding LFP features recorded from resting or movement states improved the accuracy of predicting the most satisfactory stimulating contact.…”

Section: Discussionmentioning

confidence: 99%

“…Second, the present study only identified high- β oscillations as a single feature to estimate the therapeutic outcome. Combining multiple electrophysiological features and imaging markers resulted in higher prediction accuracy than that obtained by using beta activity alone (Hirschmann et al, 2022 ; Shah et al, 2022 ). However, the use of the dynamic high- β oscillations as a single feature is more intuitive and computation saving and can be a rational target for closed-loop DBS.…”

Section: Discussionmentioning

confidence: 99%

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Subthalamic high-beta oscillation informs the outcome of deep brain stimulation in patients with Parkinson's disease

Chen

et al. 2022

Front. Hum. Neurosci.

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BackgroundThe therapeutic effect of deep brain stimulation (DBS) of the subthalamic nucleus (STN) for Parkinson's disease (PD) is related to the modulation of pathological neural activities, particularly the synchronization in the β band (13–35 Hz). However, whether the local β activity in the STN region can directly predict the stimulation outcome remains unclear.ObjectiveWe tested the hypothesis that low-β (13–20 Hz) and/or high-β (20–35 Hz) band activities recorded from the STN region can predict DBS efficacy.MethodsLocal field potentials (LFPs) were recorded in 26 patients undergoing deep brain stimulation surgery in the subthalamic nucleus area. Recordings were made after the implantation of the DBS electrode prior to its connection to a stimulator. The maximum normalized powers in the theta (4–7 Hz), alpha (7–13 Hz), low-β (13–20 Hz), high-β (20–35 Hz), and low-γ (40–55 Hz) subbands in the postoperatively recorded LFP were correlated with the stimulation-induced improvement in contralateral tremor or bradykinesia–rigidity. The distance between the contact selected for stimulation and the contact with the maximum subband power was correlated with the stimulation efficacy. Following the identification of the potential predictors by the significant correlations, a multiple regression analysis was performed to evaluate their effect on the outcome.ResultsThe maximum high-β power was positively correlated with bradykinesia–rigidity improvement (rs = 0.549, p < 0.0001). The distance to the contact with maximum high-β power was negatively correlated with bradykinesia–rigidity improvement (rs = −0.452, p < 0.001). No significant correlation was observed with low-β power. The maximum high-β power and the distance to the contact with maximum high-β power were both significant predictors for bradykinesia–rigidity improvement in the multiple regression analysis, explaining 37.4% of the variance altogether. Tremor improvement was not significantly correlated with any frequency.ConclusionHigh-β oscillations, but not low-β oscillations, recorded from the STN region with the DBS lead can inform stimulation-induced improvement in contralateral bradykinesia–rigidity in patients with PD. High-β oscillations can help refine electrode targeting and inform contact selection for DBS therapy.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Subthalamic high-beta oscillation informs the outcome of deep brain stimulation in patients with Parkinson's disease

Chen

et al. 2022

Front. Hum. Neurosci.

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“…However, due to the limited memory capacity of currently available sensing devices, the sampling rate of the recordings remains low. Consequently, the analysis of frequencies above Nyquist (>125 Hz) was not accessible, although, e.g., activity within the gamma frequency range has been established as a pro-kinetic signal [ 35 ] and might be useful to predict effective stimulation contacts [ 36 ]. Here, we only assessed the predictive power of elevated beta activity on akinetic–rigid symptoms of PD, but we did not analyze its effect on tremor and other symptoms.…”

Section: Discussionmentioning

confidence: 99%

Local Field Potential-Guided Contact Selection Using Chronically Implanted Sensing Devices for Deep Brain Stimulation in Parkinson’s Disease

et al. 2022

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Intra- and perioperatively recorded local field potential (LFP) activity of the nucleus subthalamicus (STN) has been suggested to guide contact selection in patients undergoing deep brain stimulation (DBS) for Parkinson’s disease (PD). Despite the invention of sensing capacities in chronically implanted devices, a comprehensible algorithm that enables contact selection using such recordings is still lacking. We evaluated a fully automated algorithm that uses the weighted average of bipolar recordings to determine effective monopolar contacts based on elevated activity in the beta band. LFPs from 14 hemispheres in seven PD patients with newly implanted directional DBS leads of the STN were recorded. First, the algorithm determined the stimulation level with the highest beta activity. Based on the prior determined level, the directional contact with the highest beta activity was chosen in the second step. The mean clinical efficacy of the contacts chosen using the algorithm did not statistically differ from the mean clinical efficacy of standard contact selection as performed in clinical routine. All recording sites were projected into MNI standard space to investigate the feasibility of the algorithm with respect to the anatomical boundaries of the STN. We conclude that the proposed algorithm is a first step towards LFP-based contact selection in STN-DBS for PD using chronically implanted devices.

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“…For instance, the dopamine depletion values in our model could both increase due to the progression of PD and decrease due to the action of dopamine agonists, but to proper model this latter aspect we have to take into account several other pathophysiological aspects [73]. Moreover, it would be interesting to simulate the action of Deep Brain stimulation as in [67,[74][75][76] also in our network to evaluate the input of different targets on suppressing the β oscillations and compare it to experimental results [77][78][79].…”

Section: Discussionmentioning

confidence: 99%

Dopamine depletion leads to pathological synchronization of distinct basal ganglia loops in the beta band

Ortone

Vergani

Mannella

et al. 2022

Preprint

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Motor symptoms of Parkinson's Disease (PD) are associated with dopamine deficits and pathological oscillation of basal ganglia (BG) neurons in the beta range ([12-30] Hz). However, how the dopamine depletion affects the oscillation dynamics of BG nuclei is still unclear. With a spiking neurons model, we here captured the features of BG nuclei interactions leading to oscillations in dopamine-depleted condition. We found that both the loop between subthalamic nucleus and Globus Pallidus pars externa (GPe) and the loop between striatal fast spiking and medium spiny neurons and GPe displayed resonances in the beta range, and synchronized to a common beta frequency through interaction. Crucially, the synchronization depends on dopamine depletion: the two loops were largely independent for high levels of dopamine, but progressively synchronized as dopamine was depleted due to the increased strength of the striatal loop. Our results highlight the role of the interplay between the GPe-STN and the GPe-striatum loop in generating sustained beta oscillations in PD subjects, and explain how this interplay depends on the level of dopamine. This paves the way to the design of therapies specifically addressing the onset of pathological beta oscillations.

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Combining Multimodal Biomarkers to Guide Deep Brain Stimulation Programming in Parkinson Disease

Cited by 27 publications

References 47 publications

Subthalamic high-beta oscillation informs the outcome of deep brain stimulation in patients with Parkinson's disease

Subthalamic high-beta oscillation informs the outcome of deep brain stimulation in patients with Parkinson's disease

Local Field Potential-Guided Contact Selection Using Chronically Implanted Sensing Devices for Deep Brain Stimulation in Parkinson’s Disease

Dopamine depletion leads to pathological synchronization of distinct basal ganglia loops in the beta band

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