High (130 Hz)- and mid (60 Hz)-frequency deep brain stimulation in the subthalamic nucleus differentially modulate response inhibition: A preliminary combined EEG and eye tracking study

While deep brain stimulation (DBS) in the subthalamic nucleus (STN) improves motor functions in Parkinson’s disease (PD), it may also increase impulsivity by interfering with the inhibition of reflexive responses. The aim of this study was to investigate if varying the pulse frequency of STN-DBS has...

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Main Authors: Josefine Waldthaler, Alexander Sperlich, Aylin König, Charlotte Stüssel, Frank Bremmer, Lars Timmermann, David Pedrosa
Format: Article
Language:English
Published: Elsevier 2023-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158223000037
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author Josefine Waldthaler
Alexander Sperlich
Aylin König
Charlotte Stüssel
Frank Bremmer
Lars Timmermann
David Pedrosa
author_facet Josefine Waldthaler
Alexander Sperlich
Aylin König
Charlotte Stüssel
Frank Bremmer
Lars Timmermann
David Pedrosa
author_sort Josefine Waldthaler
collection DOAJ
description While deep brain stimulation (DBS) in the subthalamic nucleus (STN) improves motor functions in Parkinson’s disease (PD), it may also increase impulsivity by interfering with the inhibition of reflexive responses. The aim of this study was to investigate if varying the pulse frequency of STN-DBS has a modulating effect on response inhibition and its neural correlates.For this purpose, 14 persons with PD repeated an antisaccade task in three stimulation settings (DBS off, high-frequency DBS (130 Hz), mid-frequency DBS (60 Hz)) in a randomized order, while eye movements and brain activity via high-density EEG were recorded.On a behavioral level, 130 Hz DBS stimulation had no effect on response inhibition measured as antisaccade error rate, while 60 Hz DBS induced a slight but significant reduction of directional errors compared with the DBS-off state and 130 Hz DBS. Further, stimulation with both frequencies decreased the onset latency of correct antisaccades, while increasing the latency of directional errors.Time-frequency domain analysis of the EEG data revealed that 60 Hz DBS was associated with an increase in preparatory theta power over a midfrontal region of interest compared with the off-DBS state which is generally regarded as a marker of increased cognitive control. While no significant differences in brain activity over mid- and lateral prefrontal regions of interest emerged between the 60 Hz and 130 Hz conditions, both stimulation frequencies were associated with a stronger midfrontal beta desynchronization during the mental preparation for correct antisaccades compared with DBS off-state which is discussed in the context of potentially enhanced proactive recruitment of the oculomotor network.Our preliminary findings suggest that mid-frequency STN-DBS may provide beneficial effects on response inhibition, while both 130 Hz- and 60 Hz STN-DBS may promote voluntary actions at the expense of slower reflexive responses.
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spelling doaj.art-29814c46b228406fb6ec7f65c592bf442023-03-16T05:04:02ZengElsevierNeuroImage: Clinical2213-15822023-01-0137103314High (130 Hz)- and mid (60 Hz)-frequency deep brain stimulation in the subthalamic nucleus differentially modulate response inhibition: A preliminary combined EEG and eye tracking studyJosefine Waldthaler0Alexander Sperlich1Aylin König2Charlotte Stüssel3Frank Bremmer4Lars Timmermann5David Pedrosa6Department of Neurology, University Hospital Giessen and Marburg, Marburg, Germany; Department of Neurology, Philipps-University Marburg, Marburg, Germany; Center for Mind, Brain, and Behavior (CMBB), Philipps-University Marburg and Justus-Liebig-University, Giessen, Germany; Corresponding author at: Department of Neurology, University of Marburg, Marburg, Germany.Department of Neurology, University Hospital Giessen and Marburg, Marburg, Germany; Department of Neurology, Philipps-University Marburg, Marburg, GermanyDepartment of Neurophysics, Philipps-University Marburg, Marburg, GermanyDepartment of Neurology, University Hospital Giessen and Marburg, Marburg, Germany; Department of Neurology, Philipps-University Marburg, Marburg, GermanyCenter for Mind, Brain, and Behavior (CMBB), Philipps-University Marburg and Justus-Liebig-University, Giessen, Germany; Department of Neurophysics, Philipps-University Marburg, Marburg, GermanyDepartment of Neurology, University Hospital Giessen and Marburg, Marburg, Germany; Department of Neurology, Philipps-University Marburg, Marburg, Germany; Center for Mind, Brain, and Behavior (CMBB), Philipps-University Marburg and Justus-Liebig-University, Giessen, GermanyDepartment of Neurology, University Hospital Giessen and Marburg, Marburg, Germany; Department of Neurology, Philipps-University Marburg, Marburg, Germany; Center for Mind, Brain, and Behavior (CMBB), Philipps-University Marburg and Justus-Liebig-University, Giessen, GermanyWhile deep brain stimulation (DBS) in the subthalamic nucleus (STN) improves motor functions in Parkinson’s disease (PD), it may also increase impulsivity by interfering with the inhibition of reflexive responses. The aim of this study was to investigate if varying the pulse frequency of STN-DBS has a modulating effect on response inhibition and its neural correlates.For this purpose, 14 persons with PD repeated an antisaccade task in three stimulation settings (DBS off, high-frequency DBS (130 Hz), mid-frequency DBS (60 Hz)) in a randomized order, while eye movements and brain activity via high-density EEG were recorded.On a behavioral level, 130 Hz DBS stimulation had no effect on response inhibition measured as antisaccade error rate, while 60 Hz DBS induced a slight but significant reduction of directional errors compared with the DBS-off state and 130 Hz DBS. Further, stimulation with both frequencies decreased the onset latency of correct antisaccades, while increasing the latency of directional errors.Time-frequency domain analysis of the EEG data revealed that 60 Hz DBS was associated with an increase in preparatory theta power over a midfrontal region of interest compared with the off-DBS state which is generally regarded as a marker of increased cognitive control. While no significant differences in brain activity over mid- and lateral prefrontal regions of interest emerged between the 60 Hz and 130 Hz conditions, both stimulation frequencies were associated with a stronger midfrontal beta desynchronization during the mental preparation for correct antisaccades compared with DBS off-state which is discussed in the context of potentially enhanced proactive recruitment of the oculomotor network.Our preliminary findings suggest that mid-frequency STN-DBS may provide beneficial effects on response inhibition, while both 130 Hz- and 60 Hz STN-DBS may promote voluntary actions at the expense of slower reflexive responses.http://www.sciencedirect.com/science/article/pii/S2213158223000037AntisaccadeResponse inhibitionParkinson’s diseaseExecutive functionsEye trackingMovement disorders
spellingShingle Josefine Waldthaler
Alexander Sperlich
Aylin König
Charlotte Stüssel
Frank Bremmer
Lars Timmermann
David Pedrosa
High (130 Hz)- and mid (60 Hz)-frequency deep brain stimulation in the subthalamic nucleus differentially modulate response inhibition: A preliminary combined EEG and eye tracking study
NeuroImage: Clinical
Antisaccade
Response inhibition
Parkinson’s disease
Executive functions
Eye tracking
Movement disorders
title High (130 Hz)- and mid (60 Hz)-frequency deep brain stimulation in the subthalamic nucleus differentially modulate response inhibition: A preliminary combined EEG and eye tracking study
title_full High (130 Hz)- and mid (60 Hz)-frequency deep brain stimulation in the subthalamic nucleus differentially modulate response inhibition: A preliminary combined EEG and eye tracking study
title_fullStr High (130 Hz)- and mid (60 Hz)-frequency deep brain stimulation in the subthalamic nucleus differentially modulate response inhibition: A preliminary combined EEG and eye tracking study
title_full_unstemmed High (130 Hz)- and mid (60 Hz)-frequency deep brain stimulation in the subthalamic nucleus differentially modulate response inhibition: A preliminary combined EEG and eye tracking study
title_short High (130 Hz)- and mid (60 Hz)-frequency deep brain stimulation in the subthalamic nucleus differentially modulate response inhibition: A preliminary combined EEG and eye tracking study
title_sort high 130 hz and mid 60 hz frequency deep brain stimulation in the subthalamic nucleus differentially modulate response inhibition a preliminary combined eeg and eye tracking study
topic Antisaccade
Response inhibition
Parkinson’s disease
Executive functions
Eye tracking
Movement disorders
url http://www.sciencedirect.com/science/article/pii/S2213158223000037
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