Directional local field potentials: A tool to optimize deep brain stimulation

Tinkhauser, Gerd; Pogosyan, Alek; Debove, Ines; Nowacki, Andreas; Shah, Syed Ahmar; Seidel, Kathleen; Tan, Huiling; Brittain, John-Stuart; Petermann, Katrin; Biase, Lazzaro di; Oertel, Markus Florian; Pollo, Claudio; Brown, Peter; Schuepbach, Michael

doi:10.1002/mds.27215

Cited by 125 publications

(127 citation statements)

References 24 publications

(48 reference statements)

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“…Contrary to this hypothesis, the present study provides compelling evidence that rather than a feature important for normal motor control, exaggerated, movement-modulated HFO activity in the GPi is in fact a pathophysiological feature of the parkinsonian condition. These findings improve our understanding of the pathophysiological role of basal ganglia high frequency oscillatory activity in Parkinson's disease and support further exploration into their functional role in the development of specific motor signs, as well as how these signals may inform DBS device programming (Horn et al, 2017;Tinkhauser et al, 2018) or the design of electrophysiological biomarker-based adaptive stimulation approaches (Meidahl et al, 2017) in patients receiving GPi…”

Section: Introductionmentioning

confidence: 58%

High-frequency oscillations in the internal globus pallidus: a pathophysiological biomarker in Parkinson's disease?

Johnson

Aman

et al. 2020

Preprint

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Abnormal oscillatory neural activity in the basal ganglia is thought to play a pathophysiological role in Parkinson's disease. Many patient studies have focused on beta frequency band local field potential activity in the subthalamic nucleus, however increasing evidence points to alterations in neural oscillations in high frequency ranges (>100 Hz) having pathophysiological relevance. Prior studies have found that power in subthalamic high frequency oscillations (HFOs) is positively correlated with dopamine tone and increased during voluntary movements, implicating these brain rhythms in normal basal ganglia function. Contrary to this idea, in the current study we present a combination of clinical and preclinical data that support the hypothesis that HFOs in the internal globus pallidus (GPi) are a pathophysiological feature of Parkinson's disease. Spontaneous and movement-related pallidal field potentials were recorded from deep brain stimulation (DBS) leads targeting the GPi in five externalized Parkinson's disease patients, on and off dopaminergic medication. We identified a prominent oscillatory peak centered at 200-300 Hz in the off-medication rest recordings in all patients. High frequency power increased during movement, and the magnitude of modulation was negatively correlated with bradykinesia.Moreover, high frequency oscillations were significantly attenuated in the on-medication condition, suggesting they are a feature of the parkinsonian condition. To further confirm that GPi high frequency oscillations are characteristic of dopamine depletion, we also collected field potentials from DBS leads chronically implanted in three rhesus monkeys before and after the induction of parkinsonism with the neurotoxin 1-methyl-4-phenyl-1,2,3,6 tetrahydropyridine (MPTP). High frequency oscillations and their modulation during movement were not prominent in the normal condition but emerged in the parkinsonian condition in the monkey model. These data provide the first evidence demonstrating that exaggerated, movement-modulated high frequency oscillations in the internal globus pallidus are a pathophysiological feature of Parkinson's disease, and motivate additional investigations into the functional roles of high frequency neural oscillations across the basal ganglia-thalamocortical motor circuit and their relationship to motor control in normal and diseased states. These findings also provide rationale for further exploration of these signals for electrophysiological biomarker-based device programming and stimulation strategies in patients receiving deep brain stimulation therapy.

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Section: Introductionmentioning

confidence: 58%

High-frequency oscillations in the internal globus pallidus: a pathophysiological biomarker in Parkinson's disease?

Johnson

Aman

et al. 2020

Preprint

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“…Past research has linked maximal beta band activity to the dorsal (motor) region of the STN , which also corresponds to the site that offers the most effective stimulation . We therefore tested whether beta suppression is particularly pronounced in the region that exhibits the strongest beta peak.…”

Section: Methodsmentioning

confidence: 99%

The Effect of Unilateral Subthalamic Nucleus Deep Brain Stimulation on Contralateral Subthalamic Nucleus Local Field Potentials

Hasegawa

Fischer

Tan

et al. 2020

Neuromodulation: Technology at the Neural Interface

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Objectives Unilateral subthalamic nucleus (STN) deep brain stimulation (DBS) for Parkinson's disease (PD) improves ipsilateral symptoms, but how this occurs is not well understood. We investigated whether unilateral STN DBS suppresses contralateral STN beta activity in the local field potential (LFP), since previous research has shown that activity in the beta band can correlate with the severity of contralateral clinical symptoms and is modulated by DBS. Materials and Methods We recorded STN LFPs from 14 patients who underwent bilateral STN DBS for PD. Following a baseline recording, unilateral STN stimulation was delivered at therapeutic parameters while LFPs were recorded from the contralateral (unstimulated) STN. Results Unilateral STN DBS suppressed contralateral beta power (p = 0.039, relative suppression = −5.7% ± [SD] 16% when averaging across the highest beta peak channels; p = 0.033, relative suppression = −5.2% ± 13% when averaging across all channels). Unilateral STN DBS produced a 17% ipsilateral (p = 0.016) and 29% contralateral (p = 0.002) improvement in upper limb hemi‐body bradykinesia‐rigidity (UPDRS‐III, items 3.3‐3.6). The ipsilateral clinical improvement and the change in contralateral beta power were not significantly correlated. Conclusions Unilateral STN DBS suppresses contralateral STN beta LFP. This indicates that unilateral STN DBS modulates bilateral basal ganglia networks. It remains unclear whether this mechanism accounts for the ipsilateral motor improvements.

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“…The practical usefulness of this technical advance however is currently limited by the time a specialized neurologist, together with the patient, must devote to conducting a thorough review of the effects of monopolar stimulation. Here, an automatic algorithm to determine the best contact combination could significantly advance the clinical adoption of directional stimulation [156][157][158].…”

Section: Electrode Designmentioning

confidence: 99%

Toward Electrophysiology-Based Intelligent Adaptive Deep Brain Stimulation for Movement Disorders

et al. 2019

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Deep brain stimulation (DBS) represents one of the major clinical breakthroughs in the age of translational neuroscience. In 1987, Benabid and colleagues demonstrated that high-frequency stimulation can mimic the effects of ablative neurosurgery in Parkinson's disease (PD), while offering two key advantages to previous procedures: adjustability and reversibility. Deep brain stimulation is now an established therapeutic approach that robustly alleviates symptoms in patients with movement disorders, such as Parkinson's disease, essential tremor, and dystonia, who present with inadequate or adverse responses to medication. Currently, stimulation electrodes are implanted in specific target regions of the basal ganglia-thalamic circuit and stimulation pulses are delivered chronically. To achieve optimal therapeutic effect, stimulation frequency, amplitude, and pulse width must be adjusted on a patient-specific basis by a movement disorders specialist. The finding that pathological neural activity can be sampled directly from the target region using the DBS electrode has inspired a novel DBS paradigm: closed-loop adaptive DBS (aDBS). The goal of this strategy is to identify pathological and physiologically normal patterns of neuronal activity that can be used to adapt stimulation parameters to the concurrent therapeutic demand. This review will give detailed insight into potential biomarkers and discuss next-generation strategies, implementing advances in artificial intelligence, to further elevate the therapeutic potential of DBS by capitalizing on its modifiable nature. Development of intelligent aDBS, with an ability to deliver highly personalized treatment regimens and to create symptom-specific therapeutic strategies in real-time, could allow for significant further improvements in the quality of life for movement disorders patients with DBS that ultimately could outperform traditional drug treatment.

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Directional local field potentials: A tool to optimize deep brain stimulation

Cited by 125 publications

References 24 publications

High-frequency oscillations in the internal globus pallidus: a pathophysiological biomarker in Parkinson's disease?

High-frequency oscillations in the internal globus pallidus: a pathophysiological biomarker in Parkinson's disease?

The Effect of Unilateral Subthalamic Nucleus Deep Brain Stimulation on Contralateral Subthalamic Nucleus Local Field Potentials

Toward Electrophysiology-Based Intelligent Adaptive Deep Brain Stimulation for Movement Disorders

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