Bilateral deep brain stimulation of the subthalamic nucleus increases pointing error during memory-guided sequential reaching

Fabian J. David; Lisa C. Goelz; Ruth Z. Tangonan; Leonard Verhagen Metman; Daniel M. Corcos

doi:10.1007/s00221-018-5197-3

Bilateral deep brain stimulation of the subthalamic nucleus increases pointing error during memory-guided sequential reaching

Fabian J. David^*, Lisa C. Goelz, Ruth Z. Tangonan, Leonard Verhagen Metman, Daniel M. Corcos

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

8 Scopus citations

Abstract

Deep brain stimulation of the subthalamic nucleus (STN DBS) significantly improves clinical motor symptoms, as well as intensive aspects of movement like velocity and amplitude in patients with Parkinson’s disease (PD). However, the effects of bilateral STN DBS on integrative and coordinative aspects of motor control are equivocal. The aim of this study was to investigate the effects of bilateral STN DBS on integrative and coordinative aspects of movement using a memory-guided sequential reaching task. The primary outcomes were eye and finger velocity and end-point error. We expected that bilateral STN DBS would increase reaching velocity. More importantly, we hypothesized that bilateral STN DBS would increase eye and finger end-point error and this would not simply be the result of a speed accuracy trade-off. Ten patients with PD and bilaterally implanted subthalamic stimulators performed a memory-guided sequential reaching task under four stimulator conditions (DBS-OFF, DBS-LEFT, DBS-RIGHT, and DBS-BILATERAL) over 4 days. DBS-BILATERAL significantly increased eye velocity compared to DBS-OFF, DBS-LEFT, and DBS-RIGHT. It also increased finger velocity compared to DBS-OFF and DBS-RIGHT. DBS-BILATERAL did not change eye end-point error. The novel finding was that DBS-BILATERAL increased finger end-point error compared to DBS-OFF, DBS-LEFT, and DBS-RIGHT even after adjusting for differences in velocity. We conclude that bilateral STN DBS may facilitate basal ganglia–cortical networks that underlie intensive aspects of movement like velocity, but it may disrupt selective basal ganglia–cortical networks that underlie certain integrative and coordinative aspects of movement such as spatial accuracy.

Original language	English (US)
Pages (from-to)	1053-1065
Number of pages	13
Journal	Experimental Brain Research
Volume	236
Issue number	4
DOIs	https://doi.org/10.1007/s00221-018-5197-3
State	Published - Apr 1 2018

Funding

Conflict of interest FJD, RZT, and LCG have nothing to report. DMC is a Full Professor at Northwestern University and receives a salary, has additional NIH funding (5R01NS074343, 5R01HD075777, 1R01DK110699, 5T15HD074546), and receives honoraria and/or consults for the following: University of Florida, Ohio University Athens, Temple University, Iowa State University, University of Alabama, Birmingham, Oregon Health Sciences Institute, University of Westminster, University of Waterloo, University of Colorado, Denver, Several NIH Study Sections, ACRM, ASNR, University of New Hampshire, University of Minnesota, Movement Disorders Society. LVM has foundation research support from Michael J. Fox Foundation; commercial research support from Medtronic, Inc., US World-Meds LLC, Pfizer Inc, Boston Scientific, Avanir Pharmaceuticals, Inc., and Adamas Pharmaceuticals, Inc.; is on the scientific advisory board of St. Jude Medical, AbbVie, Inc., and Britannia Pharmaceuticals Ltd.; and consults for St. Jude Medical, AbbVie, Inc., Medtronic, Inc., and Boston Scientific. Funding This study was supported by National Institutes of Health (R56NS040902 and R01NS09295001). The sponsors were not involved in the design, conduct, collection, management, analysis, and/or interpretation of the study results and preparation, review, or approval of the manuscript. The views expressed in this article are those of the authors and do not necessarily reflect the position or policy of NIH. Statistical analysis: Conducted by FJD. The authors thank the participants and our professional colleagues, Maya Cottongim, and Christiane Alford for their important contributions to the successful implementation of this project. Lisa C. Goelz is equally credited as first author. FJD, RZT, and LCG have nothing to report. DMC is a Full Professor at Northwestern University and receives a salary, has additional NIH funding (5R01NS074343, 5R01HD075777, 1R01DK110699, 5T15HD074546), and receives honoraria and/or consults for the following: University of Florida, Ohio University Athens, Temple University, Iowa State University, University of Alabama, Birmingham, Oregon Health Sciences Institute, University of Westminster, University of Waterloo, University of Colorado, Denver, Several NIH Study Sections, ACRM, ASNR, University of New Hampshire, University of Minnesota, Movement Disorders Society. LVM has foundation research support from Michael J. Fox Foundation; commercial research support from Medtronic, Inc., US WorldMeds LLC, Pfizer Inc, Boston Scientific, Avanir Pharmaceuticals, Inc., and Adamas Pharmaceuticals, Inc.; is on the scientific advisory board of St. Jude Medical, AbbVie, Inc., and Britannia Pharmaceuticals Ltd.; and consults for St. Jude Medical, AbbVie, Inc., Medtronic, Inc., and Boston Scientific.

Keywords

Deep brain stimulation
Memory-guided
Parkinson disease
STN DBS
Sequential reach
Subthalamic nucleus

ASJC Scopus subject areas

General Neuroscience

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10.1007/s00221-018-5197-3

Cite this

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title = "Bilateral deep brain stimulation of the subthalamic nucleus increases pointing error during memory-guided sequential reaching",

abstract = "Deep brain stimulation of the subthalamic nucleus (STN DBS) significantly improves clinical motor symptoms, as well as intensive aspects of movement like velocity and amplitude in patients with Parkinson{\textquoteright}s disease (PD). However, the effects of bilateral STN DBS on integrative and coordinative aspects of motor control are equivocal. The aim of this study was to investigate the effects of bilateral STN DBS on integrative and coordinative aspects of movement using a memory-guided sequential reaching task. The primary outcomes were eye and finger velocity and end-point error. We expected that bilateral STN DBS would increase reaching velocity. More importantly, we hypothesized that bilateral STN DBS would increase eye and finger end-point error and this would not simply be the result of a speed accuracy trade-off. Ten patients with PD and bilaterally implanted subthalamic stimulators performed a memory-guided sequential reaching task under four stimulator conditions (DBS-OFF, DBS-LEFT, DBS-RIGHT, and DBS-BILATERAL) over 4 days. DBS-BILATERAL significantly increased eye velocity compared to DBS-OFF, DBS-LEFT, and DBS-RIGHT. It also increased finger velocity compared to DBS-OFF and DBS-RIGHT. DBS-BILATERAL did not change eye end-point error. The novel finding was that DBS-BILATERAL increased finger end-point error compared to DBS-OFF, DBS-LEFT, and DBS-RIGHT even after adjusting for differences in velocity. We conclude that bilateral STN DBS may facilitate basal ganglia–cortical networks that underlie intensive aspects of movement like velocity, but it may disrupt selective basal ganglia–cortical networks that underlie certain integrative and coordinative aspects of movement such as spatial accuracy.",

keywords = "Deep brain stimulation, Memory-guided, Parkinson disease, STN DBS, Sequential reach, Subthalamic nucleus",

author = "David, {Fabian J.} and Goelz, {Lisa C.} and Tangonan, {Ruth Z.} and Metman, {Leonard Verhagen} and Corcos, {Daniel M.}",

note = "Funding Information: Conflict of interest FJD, RZT, and LCG have nothing to report. DMC is a Full Professor at Northwestern University and receives a salary, has additional NIH funding (5R01NS074343, 5R01HD075777, 1R01DK110699, 5T15HD074546), and receives honoraria and/or consults for the following: University of Florida, Ohio University Athens, Temple University, Iowa State University, University of Alabama, Birmingham, Oregon Health Sciences Institute, University of Westminster, University of Waterloo, University of Colorado, Denver, Several NIH Study Sections, ACRM, ASNR, University of New Hampshire, University of Minnesota, Movement Disorders Society. LVM has foundation research support from Michael J. Fox Foundation; commercial research support from Medtronic, Inc., US World-Meds LLC, Pfizer Inc, Boston Scientific, Avanir Pharmaceuticals, Inc., and Adamas Pharmaceuticals, Inc.; is on the scientific advisory board of St. Jude Medical, AbbVie, Inc., and Britannia Pharmaceuticals Ltd.; and consults for St. Jude Medical, AbbVie, Inc., Medtronic, Inc., and Boston Scientific. Funding Information: Funding This study was supported by National Institutes of Health (R56NS040902 and R01NS09295001). The sponsors were not involved in the design, conduct, collection, management, analysis, and/or interpretation of the study results and preparation, review, or approval of the manuscript. The views expressed in this article are those of the authors and do not necessarily reflect the position or policy of NIH. Statistical analysis: Conducted by FJD. Funding Information: The authors thank the participants and our professional colleagues, Maya Cottongim, and Christiane Alford for their important contributions to the successful implementation of this project. Lisa C. Goelz is equally credited as first author. FJD, RZT, and LCG have nothing to report. DMC is a Full Professor at Northwestern University and receives a salary, has additional NIH funding (5R01NS074343, 5R01HD075777, 1R01DK110699, 5T15HD074546), and receives honoraria and/or consults for the following: University of Florida, Ohio University Athens, Temple University, Iowa State University, University of Alabama, Birmingham, Oregon Health Sciences Institute, University of Westminster, University of Waterloo, University of Colorado, Denver, Several NIH Study Sections, ACRM, ASNR, University of New Hampshire, University of Minnesota, Movement Disorders Society. LVM has foundation research support from Michael J. Fox Foundation; commercial research support from Medtronic, Inc., US WorldMeds LLC, Pfizer Inc, Boston Scientific, Avanir Pharmaceuticals, Inc., and Adamas Pharmaceuticals, Inc.; is on the scientific advisory board of St. Jude Medical, AbbVie, Inc., and Britannia Pharmaceuticals Ltd.; and consults for St. Jude Medical, AbbVie, Inc., Medtronic, Inc., and Boston Scientific. Publisher Copyright: {\textcopyright} 2018, Springer-Verlag GmbH Germany, part of Springer Nature.",

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doi = "10.1007/s00221-018-5197-3",

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AU - Goelz, Lisa C.

AU - Tangonan, Ruth Z.

AU - Metman, Leonard Verhagen

AU - Corcos, Daniel M.

N1 - Funding Information: Conflict of interest FJD, RZT, and LCG have nothing to report. DMC is a Full Professor at Northwestern University and receives a salary, has additional NIH funding (5R01NS074343, 5R01HD075777, 1R01DK110699, 5T15HD074546), and receives honoraria and/or consults for the following: University of Florida, Ohio University Athens, Temple University, Iowa State University, University of Alabama, Birmingham, Oregon Health Sciences Institute, University of Westminster, University of Waterloo, University of Colorado, Denver, Several NIH Study Sections, ACRM, ASNR, University of New Hampshire, University of Minnesota, Movement Disorders Society. LVM has foundation research support from Michael J. Fox Foundation; commercial research support from Medtronic, Inc., US World-Meds LLC, Pfizer Inc, Boston Scientific, Avanir Pharmaceuticals, Inc., and Adamas Pharmaceuticals, Inc.; is on the scientific advisory board of St. Jude Medical, AbbVie, Inc., and Britannia Pharmaceuticals Ltd.; and consults for St. Jude Medical, AbbVie, Inc., Medtronic, Inc., and Boston Scientific. Funding Information: Funding This study was supported by National Institutes of Health (R56NS040902 and R01NS09295001). The sponsors were not involved in the design, conduct, collection, management, analysis, and/or interpretation of the study results and preparation, review, or approval of the manuscript. The views expressed in this article are those of the authors and do not necessarily reflect the position or policy of NIH. Statistical analysis: Conducted by FJD. Funding Information: The authors thank the participants and our professional colleagues, Maya Cottongim, and Christiane Alford for their important contributions to the successful implementation of this project. Lisa C. Goelz is equally credited as first author. FJD, RZT, and LCG have nothing to report. DMC is a Full Professor at Northwestern University and receives a salary, has additional NIH funding (5R01NS074343, 5R01HD075777, 1R01DK110699, 5T15HD074546), and receives honoraria and/or consults for the following: University of Florida, Ohio University Athens, Temple University, Iowa State University, University of Alabama, Birmingham, Oregon Health Sciences Institute, University of Westminster, University of Waterloo, University of Colorado, Denver, Several NIH Study Sections, ACRM, ASNR, University of New Hampshire, University of Minnesota, Movement Disorders Society. LVM has foundation research support from Michael J. Fox Foundation; commercial research support from Medtronic, Inc., US WorldMeds LLC, Pfizer Inc, Boston Scientific, Avanir Pharmaceuticals, Inc., and Adamas Pharmaceuticals, Inc.; is on the scientific advisory board of St. Jude Medical, AbbVie, Inc., and Britannia Pharmaceuticals Ltd.; and consults for St. Jude Medical, AbbVie, Inc., Medtronic, Inc., and Boston Scientific. Publisher Copyright: © 2018, Springer-Verlag GmbH Germany, part of Springer Nature.

PY - 2018/4/1

Y1 - 2018/4/1

N2 - Deep brain stimulation of the subthalamic nucleus (STN DBS) significantly improves clinical motor symptoms, as well as intensive aspects of movement like velocity and amplitude in patients with Parkinson’s disease (PD). However, the effects of bilateral STN DBS on integrative and coordinative aspects of motor control are equivocal. The aim of this study was to investigate the effects of bilateral STN DBS on integrative and coordinative aspects of movement using a memory-guided sequential reaching task. The primary outcomes were eye and finger velocity and end-point error. We expected that bilateral STN DBS would increase reaching velocity. More importantly, we hypothesized that bilateral STN DBS would increase eye and finger end-point error and this would not simply be the result of a speed accuracy trade-off. Ten patients with PD and bilaterally implanted subthalamic stimulators performed a memory-guided sequential reaching task under four stimulator conditions (DBS-OFF, DBS-LEFT, DBS-RIGHT, and DBS-BILATERAL) over 4 days. DBS-BILATERAL significantly increased eye velocity compared to DBS-OFF, DBS-LEFT, and DBS-RIGHT. It also increased finger velocity compared to DBS-OFF and DBS-RIGHT. DBS-BILATERAL did not change eye end-point error. The novel finding was that DBS-BILATERAL increased finger end-point error compared to DBS-OFF, DBS-LEFT, and DBS-RIGHT even after adjusting for differences in velocity. We conclude that bilateral STN DBS may facilitate basal ganglia–cortical networks that underlie intensive aspects of movement like velocity, but it may disrupt selective basal ganglia–cortical networks that underlie certain integrative and coordinative aspects of movement such as spatial accuracy.

AB - Deep brain stimulation of the subthalamic nucleus (STN DBS) significantly improves clinical motor symptoms, as well as intensive aspects of movement like velocity and amplitude in patients with Parkinson’s disease (PD). However, the effects of bilateral STN DBS on integrative and coordinative aspects of motor control are equivocal. The aim of this study was to investigate the effects of bilateral STN DBS on integrative and coordinative aspects of movement using a memory-guided sequential reaching task. The primary outcomes were eye and finger velocity and end-point error. We expected that bilateral STN DBS would increase reaching velocity. More importantly, we hypothesized that bilateral STN DBS would increase eye and finger end-point error and this would not simply be the result of a speed accuracy trade-off. Ten patients with PD and bilaterally implanted subthalamic stimulators performed a memory-guided sequential reaching task under four stimulator conditions (DBS-OFF, DBS-LEFT, DBS-RIGHT, and DBS-BILATERAL) over 4 days. DBS-BILATERAL significantly increased eye velocity compared to DBS-OFF, DBS-LEFT, and DBS-RIGHT. It also increased finger velocity compared to DBS-OFF and DBS-RIGHT. DBS-BILATERAL did not change eye end-point error. The novel finding was that DBS-BILATERAL increased finger end-point error compared to DBS-OFF, DBS-LEFT, and DBS-RIGHT even after adjusting for differences in velocity. We conclude that bilateral STN DBS may facilitate basal ganglia–cortical networks that underlie intensive aspects of movement like velocity, but it may disrupt selective basal ganglia–cortical networks that underlie certain integrative and coordinative aspects of movement such as spatial accuracy.

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Bilateral deep brain stimulation of the subthalamic nucleus increases pointing error during memory-guided sequential reaching

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