Directional deep brain stimulation leads reveal spatially distinct oscillatory activity in the globus pallidus internus of Parkinson's disease patients

Aman, Joshua E.; Johnson, Luke A.; Sanabria, David Escobar; Wang, Jing; Patriat, Rémi; Hill, Meghan; Marshall, Ethan A.; MacKinnon, Colum D.; Cooper, Scott E.; Schrock, Lauren E.; Park, Michael C.; Harel, Noam; Vitek, Jerrold L.

doi:10.1016/j.nbd.2020.104819

Cited by 31 publications

(49 citation statements)

References 24 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Insert Table 1 here Details of the surgical procedures for GPi DBS implantation and lead externalization are described in detail in a previous publication (Aman et al, 2020). Briefly, patients underwent standard 3T MRI (all patients) and a high resolution 7T MRI (4/5 patients, excluding Pt 3) for direct targeting and postoperative lead localization Patriat et al, 2018).…”

Section: Data Collection In Pd Patientsmentioning

confidence: 99%

“…In all patients a directional "1-3-3-1" electrode was used (4/5 patients: Abbott Infinity model 6172, illustrated in Figure 1C; 1/5 patients: Boston Scientific Vercise Cartesia model DB-2202-45; both leads had 1.5 mm contact height with 0.5 mm vertical spacing). After implantation the lead extension was tunneled to a subcutaneous pocket in the chest and then connected to another extension externalized at the abdomen (Aman et al, 2020).…”

Section: Data Collection In Pd Patientsmentioning

confidence: 99%

“…signal subtraction) of vertically adjacent DBS contacts within the GPi. In PD patients, only the segmented contacts of the 1-3-3-1 directional lead were used; the bipolar pair that faced the posterolateral "sensorimotor" territory was chosen for subsequent analysis (see Figure 1C, Aman et al, 2020). In patient 4 the anteromedial bipolar pair was used for analysis since this pair had higher signal to noise ratio than the other contact pairs.…”

Section: Data Analysis and Statisticsmentioning

confidence: 99%

“…We recognize that the frequency range of HFOs is not universally defined; we have chosen to define HFOs in the 100-300Hz range empirically based on our data set to encompass the spectral peaks observed in our recordings, typically centered near 200Hz. Off medication data in patients 1, 2, and 5 were included in a previous publication (Aman et al, 2020), focusing on spatial topography of resting and movement-related low frequency (5-40Hz) activity rather than HFOs as in the present study.…”

Section: Data Analysis and Statisticsmentioning

confidence: 99%

“…Despite the fact that the internal globus pallidus (GPi) is increasingly being targeted for DBS in PD patients, there are relatively few reports exploring LFP activity in the pallidum (Priori et al, 2002;Silberstein et al, 2003;Tsiokos et al, 2013Tsiokos et al, , 2017AuYong et al, 2018;Aman et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

See 4 more Smart Citations

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

Johnson

Aman

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

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.

show abstract

Section: Data Collection In Pd Patientsmentioning

confidence: 99%

Section: Data Collection In Pd Patientsmentioning

confidence: 99%

Section: Data Analysis and Statisticsmentioning

confidence: 99%

Section: Data Analysis and Statisticsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

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

Johnson

Aman

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

High‐Frequency Oscillations in the Pallidum: A Pathophysiological Biomarker in Parkinson's Disease?

Johnson

Aman

et al. 2021

Movement Disorders

Self Cite

View full text Add to dashboard Cite

A BS TRACT: Background: Abnormal oscillatory neural activity in the beta-frequency band (13-35 Hz) is thought to play a role in Parkinson's disease (PD); however, increasing evidence points to alterations in high-frequency ranges (>100 Hz) also having pathophysiological relevance. Objectives: Studies have found that power in subthalamic nucleus (STN) high-frequency oscillations is increased with dopaminergic medication and during voluntary movements, implicating these brain rhythms in normal basal ganglia function. The objective of this study was to investigate whether similar signaling occurs in the internal globus pallidus (GPi), a nucleus increasingly used as a target for deep brain stimulation (DBS) for PD. Methods: Spontaneous and movement-related GPi field potentials were recorded from DBS leads in 5 externalized PD patients on and off dopaminergic medication, as well as from 3 rhesus monkeys before and after the induction of parkinsonism with the neurotoxin 1-methyl-4-phenyl-1,2,3,6 tetrahydropyridine. Results: In the parkinsonian condition, we identified a prominent oscillatory peak centered at 200-300 Hz that increased during movement. In patients the magnitude of highfrequency oscillation modulation was negatively correlated with bradykinesia. In monkeys, high-frequency oscillations were mostly absent in the naive condition but emerged after the neurotoxin 1-methyl-4-phenyl-1,2,3,6 tetrahydropyridine. In patients, spontaneous high-frequency oscillations were significantly attenuated on-medication. Conclusions: Our findings provide evidence in support of the hypothesis that exaggerated, movementmodulated high-frequency oscillations in the GPi are pathophysiological features of PD. These findings suggest that the functional role(s) of high-frequency oscillations may differ between the STN and GPi and motivate additional investigations into their relationship to motor control in normal and diseased states.

show abstract

Paradoxical Modulation of STN β‐Band Activity with Medication Compared to Deep Brain Stimulation

Hill,

Johnson,

Wang

et al. 2023

Movement Disorders

Self Cite

View full text Add to dashboard Cite

BackgroundExcessive subthalamic nucleus (STN) β‐band (13–35 Hz) synchronized oscillations has garnered interest as a biomarker for characterizing disease state and developing adaptive stimulation systems for Parkinson's disease (PD).ObjectivesTo report on a patient with abnormal treatment‐responsive modulation in the β‐band.MethodsWe examined STN local field potentials from an externalized deep brain stimulation (DBS) lead while assessing PD motor signs in four conditions (OFF, MEDS, DBS, and MEDS+DBS).ResultsThe patient presented here exhibited a paradoxical increase in β power following administration of levodopa and pramipexole (MEDS), but an attenuation in β power during DBS and MEDS+DBS despite clinical improvement of 50% or greater under all three therapeutic conditions.ConclusionsThis case highlights the need for further study on the role of β oscillations in the pathophysiology of PD and the importance of personalized approaches to the development of β or other biomarker‐based DBS closed loop algorithms. © 2023 The Authors. Movement Disorders published by Wiley Periodicals LLC on behalf of International Parkinson and Movement Disorder Society.

show abstract

Directional deep brain stimulation leads reveal spatially distinct oscillatory activity in the globus pallidus internus of Parkinson's disease patients

Cited by 31 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?

High‐Frequency Oscillations in the Pallidum: A Pathophysiological Biomarker in Parkinson's Disease?

Paradoxical Modulation of STN β‐Band Activity with Medication Compared to Deep Brain Stimulation

Contact Info

Product

Resources

About