Theoretical Analysis of the Local Field Potential in Deep Brain Stimulation Applications

Scott F Lempka,Cameron C Mcintyre,Natasha M Maurits

doi:10.1371/journal.pone.0059839

Scott F Lempka, Cameron C Mcintyre + Show 1 more

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https://doi.org/10.1371/journal.pone.0059839

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Journal: PloS one	Publication Date: Mar 28, 2013
Citations: 138	License type: CC BY 4.0

Affiliation: Cleveland Clinic

Abstract

Deep brain stimulation (DBS) is a common therapy for treating movement disorders, such as Parkinson’s disease (PD), and provides a unique opportunity to study the neural activity of various subcortical structures in human patients. Local field potential (LFP) recordings are often performed with either intraoperative microelectrodes or DBS leads and reflect oscillatory activity within nuclei of the basal ganglia. These LFP recordings have numerous clinical implications and might someday be used to optimize DBS outcomes in closed-loop systems. However, the origin of the recorded LFP is poorly understood. Therefore, the goal of this study was to theoretically analyze LFP recordings within the context of clinical DBS applications. This goal was achieved with a detailed recording model of beta oscillations (∼20 Hz) in the subthalamic nucleus. The recording model consisted of finite element models of intraoperative microelectrodes and DBS macroelectrodes implanted in the brain along with multi-compartment cable models of STN projection neurons. Model analysis permitted systematic investigation into a number of variables that can affect the composition of the recorded LFP (e.g. electrode size, electrode impedance, recording configuration, and filtering effects of the brain, electrode-electrolyte interface, and recording electronics). The results of the study suggest that the spatial reach of the LFP can extend several millimeters. Model analysis also showed that variables such as electrode geometry and recording configuration can have a significant effect on LFP amplitude and spatial reach, while the effects of other variables, such as electrode impedance, are often negligible. The results of this study provide insight into the origin of the LFP and identify variables that need to be considered when analyzing LFP recordings in clinical DBS applications.

Highlights

While a debate continues on the exact mechanisms producing the motor symptoms of Parkinson’s disease (PD), one current hypothesis is that symptoms arise at least partially from hypersynchronous neural activity in several nuclei of the BG, including the subthalamic nucleus (STN) and the internal segment of the globus pallidus (GPi) [1]
The recording model accounted for the frequency-dependent properties of the bulk brain tissue, inhomogeneities in the tissue local to the recording electrode, the electrode-electrolyte interface (EEI), and the recording electronics
local field potential (LFP) recordings for each model were generated for a spherical population of neurons with a radius of 5 mm that contained a total of 62,276 neurons

Summary

Introduction

While a debate continues on the exact mechanisms producing the motor symptoms of Parkinson’s disease (PD), one current hypothesis is that symptoms arise at least partially from hypersynchronous neural activity in several nuclei of the BG, including the subthalamic nucleus (STN) and the internal segment of the globus pallidus (GPi) [1]. Electrophysiological local field potential (LFP) recordings with intraoperative microelectrodes or deep brain stimulation (DBS) macroelectrodes, have shown prominent oscillatory activity within a specific frequency range, e.g. 13–30 Hz, termed the beta frequency band. This beta-band activity is temporally coupled between the STN and GPi, as well as between these nuclei and various cortical regions [2]. The LFP is complementary to action potential information and single-unit and multi-unit recordings have demonstrated exaggerated activity and synchrony in the STN that are often coupled to oscillations in the LFP [5,11,12] These observations are consistent with the concept that the LFP reflects synchronized activity in a population of local neurons and their inputs [13]. Because betaband hypersynchrony in the BG exists chronically, LFP recordings from chronically-implanted DBS electrodes have been proposed as a possible control signal for closed-loop control of DBS [19,20,21,22]

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