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

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

doi:10.1016/j.nbd.2020.104819

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

Neurobiol Dis. 2020 Jun:139:104819. doi: 10.1016/j.nbd.2020.104819. Epub 2020 Feb 20.

Authors

Affiliations

¹ Department of Neurology, University of Minnesota, 516 Delaware Street SE, 12-100 Phillips Wangensteen Building, Minneapolis, MN, USA. Electronic address: aman0038@umn.edu.
² Department of Neurology, University of Minnesota, 516 Delaware Street SE, 12-100 Phillips Wangensteen Building, Minneapolis, MN, USA. Electronic address: joh03032@umn.edu.
³ Department of Neurology, University of Minnesota, 516 Delaware Street SE, 12-100 Phillips Wangensteen Building, Minneapolis, MN, USA. Electronic address: descobar@umn.edu.
⁴ Department of Neurology, University of Minnesota, 516 Delaware Street SE, 12-100 Phillips Wangensteen Building, Minneapolis, MN, USA. Electronic address: wang3444@umn.edu.
⁵ Center for Magnetic Resonance Research, Department of Radiology, University of Minnesota, 20216th Street SE, Minneapolis, MN, USA. Electronic address: patri108@morris.umn.edu.
⁶ Department of Neurology, University of Minnesota, 516 Delaware Street SE, 12-100 Phillips Wangensteen Building, Minneapolis, MN, USA. Electronic address: hillx620@umn.edu.
⁷ Department of Neurology, University of Minnesota, 516 Delaware Street SE, 12-100 Phillips Wangensteen Building, Minneapolis, MN, USA. Electronic address: marsh879@umn.edu.
⁸ Department of Neurology, University of Minnesota, 516 Delaware Street SE, 12-100 Phillips Wangensteen Building, Minneapolis, MN, USA. Electronic address: cmackinn@umn.edu.
⁹ Department of Neurology, University of Minnesota, 516 Delaware Street SE, 12-100 Phillips Wangensteen Building, Minneapolis, MN, USA. Electronic address: secooper@umn.edu.
¹⁰ Department of Neurology, University of Minnesota, 516 Delaware Street SE, 12-100 Phillips Wangensteen Building, Minneapolis, MN, USA. Electronic address: lschrock@umn.edu.
¹¹ Department of Neurosurgery, University of Minnesota, 420 Delaware Street SE, Minneapolis, MN, USA. Electronic address: mcpark@umn.edu.
¹² Center for Magnetic Resonance Research, Department of Radiology, University of Minnesota, 20216th Street SE, Minneapolis, MN, USA; Department of Neurosurgery, University of Minnesota, 420 Delaware Street SE, Minneapolis, MN, USA. Electronic address: harel002@umn.edu.
¹³ Department of Neurology, University of Minnesota, 516 Delaware Street SE, 12-100 Phillips Wangensteen Building, Minneapolis, MN, USA. Electronic address: vitek004@umn.edu.

Abstract

The goal of this study was to characterize the spectral characteristics and spatial topography of local field potential (LFP) activity in the internal segment of the globus pallidus (GPi) in patients with Parkinson's disease utilizing directional (segmented) deep brain stimulation (dDBS) leads. Data were collected from externalized dDBS leads of three patients with idiopathic Parkinson's disease after overnight withdrawal of parkinsonian medication at rest and during a cued reach-to-target task. Oscillatory activity across lead contacts/segments was examined in the context of lead locations and contact orientations determined using co-registered preoperative 7 Tesla (T) MRI and postoperative CT scans. Each of the three patients displayed a unique frequency spectrum of oscillatory activity in the pallidum, with prominent peaks ranging from 5 to 35 Hz, that modulated variably across subjects during volitional movement. Despite subject-specific spectral profiles, a consistent finding across patients was that oscillatory power was strongest and had the largest magnitude of modulation during movement in LFPs recorded from segments facing the postero-lateral "sensorimotor" region of GPi, whereas antero-medially-directed segmented contacts facing the internal capsule and/or anterior GPi, had relatively weaker LFP power and less modulation in the 5 to 35 Hz. In each subject, contact configurations chosen for clinically therapeutic stimulation (following data collection and blinded to physiology recordings), were in concordance with the contact pairs showing the largest amplitude of LFP oscillations in the 5-35 Hz range. Although limited to three subjects, these findings provide support for the hypothesis that the sensorimotor territory of the GPi corresponds to the site of maximal power of oscillatory activity in the 5 to 35 Hz and provides the greatest benefit in motor signs during stimulation in the GPi. Variability in oscillatory activity across patients is likely related to Parkinson's disease phenotype as well as small differences in recording location (i.e. lead location), highlighting the importance of lead location for optimizing stimulation efficacy. These data also provide compelling evidence for the use of LFP activity for the development of predictive stimulation models that may optimize patient benefits while reducing clinic time needed for programming.

Keywords: DBS; GPi; Local field potential; Parkinson's disease; Segmented.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Action Potentials / physiology
Beta Rhythm / physiology
Deep Brain Stimulation / methods*
Female
Globus Pallidus / physiopathology*
Humans
Magnetic Resonance Imaging
Male
Middle Aged
Parkinson Disease / physiopathology
Parkinson Disease / therapy*

Abstract

Publication types

MeSH terms

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