Neurophysiological Correlates of Gait in the Human Basal Ganglia and the PPN Region in Parkinson’s Disease
This study aimed to characterize the neurophysiological correlates of gait in the human pedunculopontine nucleus (PPN) region and the globus pallidus internus (GPi) in Parkinson's disease (PD) cohort. Though much is known about the PPN region through animal studies, there are limited physiologi...
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| Published in | Frontiers in human neuroscience Vol. 14; p. 194 |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Switzerland
Frontiers Research Foundation
04.06.2020
Frontiers Media S.A |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1662-5161 1662-5161 |
| DOI | 10.3389/fnhum.2020.00194 |
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| Abstract | This study aimed to characterize the neurophysiological correlates of gait in the human pedunculopontine nucleus (PPN) region and the globus pallidus internus (GPi) in Parkinson's disease (PD) cohort. Though much is known about the PPN region through animal studies, there are limited physiological recordings from ambulatory humans. The PPN has recently garnered interest as a potential deep brain stimulation (DBS) target for improving gait and freezing of gait (FoG) in PD. We used bidirectional neurostimulators to record from the human PPN region and GPi in a small cohort of severely affected PD subjects with FoG despite optimized dopaminergic medications. Five subjects, with confirmed on-dopaminergic medication FoG, were implanted with bilateral GPi and bilateral PPN region DBS electrodes. Electrophysiological recordings were obtained during various gait tasks for 5 months postoperatively in both the off- and on-medication conditions (obtained during the no stimulation condition). The results revealed suppression of low beta power in the GPi and a 1-8 Hz modulation in the PPN region which correlated with human gait. The PPN feature correlated with walking speed. GPi beta desynchronization and PPN low-frequency synchronization were observed as subjects progressed from rest to ambulatory tasks. Our findings add to our understanding of the neurophysiology underpinning gait and will likely contribute to the development of novel therapies for abnormal gait in PD.
Clinicaltrials.gov identifier; NCT02318927. |
|---|---|
| AbstractList | This study aimed to characterize the neurophysiological correlates of gait in the human pedunculopontine nucleus (PPN) region and the globus pallidus internus (GPi) in Parkinson’s disease (PD) cohort. Though much is known about the PPN region through animal studies, there are limited physiological recordings from ambulatory humans. The PPN has recently garnered interest as a potential deep brain stimulation (DBS) target for improving gait and freezing of gait (FoG) in PD. We used bidirectional neurostimulators to record from the human PPN region and GPi in a small cohort of severely affected PD subjects with FoG despite optimized dopaminergic medications. Five subjects, with confirmed on-dopaminergic medication FoG, were implanted with bilateral GPi and bilateral PPN region DBS electrodes. Electrophysiological recordings were obtained during various gait tasks for 5 months postoperatively in both the off- and on-medication conditions (obtained during the no stimulation condition). The results revealed suppression of low beta power in the GPi and a 1–8 Hz modulation in the PPN region which correlated with human gait. The PPN feature correlated with walking speed. GPi beta desynchronization and PPN low-frequency synchronization were observed as subjects progressed from rest to ambulatory tasks. Our findings add to our understanding of the neurophysiology underpinning gait and will likely contribute to the development of novel therapies for abnormal gait in PD.Clinical Trial Registration:Clinicaltrials.gov identifier; NCT02318927. This study aimed to characterize the neurophysiological correlates of gait in the human pedunculopontine nucleus (PPN) region and the globus pallidus internus (GPi) in Parkinson's disease (PD) cohort. Though much is known about the PPN region through animal studies, there are limited physiological recordings from ambulatory humans. The PPN has recently garnered interest as a potential deep brain stimulation (DBS) target for improving gait and freezing of gait (FoG) in PD. We used bidirectional neurostimulators to record from the human PPN region and GPi in a small cohort of severely affected PD subjects with FoG despite optimized dopaminergic medications. Five subjects, with confirmed on-dopaminergic medication FoG, were implanted with bilateral GPi and bilateral PPN region DBS electrodes. Electrophysiological recordings were obtained during various gait tasks for 5 months postoperatively in both the off- and on-medication conditions (obtained during the no stimulation condition). The results revealed suppression of low beta power in the GPi and a 1-8 Hz modulation in the PPN region which correlated with human gait. The PPN feature correlated with walking speed. GPi beta desynchronization and PPN low-frequency synchronization were observed as subjects progressed from rest to ambulatory tasks. Our findings add to our understanding of the neurophysiology underpinning gait and will likely contribute to the development of novel therapies for abnormal gait in PD. Clinical Trial Registration: Clinicaltrials.gov identifier; NCT02318927.This study aimed to characterize the neurophysiological correlates of gait in the human pedunculopontine nucleus (PPN) region and the globus pallidus internus (GPi) in Parkinson's disease (PD) cohort. Though much is known about the PPN region through animal studies, there are limited physiological recordings from ambulatory humans. The PPN has recently garnered interest as a potential deep brain stimulation (DBS) target for improving gait and freezing of gait (FoG) in PD. We used bidirectional neurostimulators to record from the human PPN region and GPi in a small cohort of severely affected PD subjects with FoG despite optimized dopaminergic medications. Five subjects, with confirmed on-dopaminergic medication FoG, were implanted with bilateral GPi and bilateral PPN region DBS electrodes. Electrophysiological recordings were obtained during various gait tasks for 5 months postoperatively in both the off- and on-medication conditions (obtained during the no stimulation condition). The results revealed suppression of low beta power in the GPi and a 1-8 Hz modulation in the PPN region which correlated with human gait. The PPN feature correlated with walking speed. GPi beta desynchronization and PPN low-frequency synchronization were observed as subjects progressed from rest to ambulatory tasks. Our findings add to our understanding of the neurophysiology underpinning gait and will likely contribute to the development of novel therapies for abnormal gait in PD. Clinical Trial Registration: Clinicaltrials.gov identifier; NCT02318927. This study aimed to characterize the neurophysiological correlates of gait in the human pedunculopontine nucleus (PPN) region and the globus pallidus internus (GPi) in Parkinson's disease (PD) cohort. Though much is known about the PPN region through animal studies, there are limited physiological recordings from ambulatory humans. The PPN has recently garnered interest as a potential deep brain stimulation (DBS) target for improving gait and freezing of gait (FoG) in PD. We used bidirectional neurostimulators to record from the human PPN region and GPi in a small cohort of severely affected PD subjects with FoG despite optimized dopaminergic medications. Five subjects, with confirmed on-dopaminergic medication FoG, were implanted with bilateral GPi and bilateral PPN region DBS electrodes. Electrophysiological recordings were obtained during various gait tasks for 5 months postoperatively in both the off- and on-medication conditions (obtained during the no stimulation condition). The results revealed suppression of low beta power in the GPi and a 1-8 Hz modulation in the PPN region which correlated with human gait. The PPN feature correlated with walking speed. GPi beta desynchronization and PPN low-frequency synchronization were observed as subjects progressed from rest to ambulatory tasks. Our findings add to our understanding of the neurophysiology underpinning gait and will likely contribute to the development of novel therapies for abnormal gait in PD. Clinicaltrials.gov identifier; NCT02318927. This study aimed to characterize the neurophysiological correlates of gait in the human pedunculopontine nucleus (PPN) region and the globus pallidus internus (GPi) in Parkinson’s disease (PD) cohort. Though much is known about the PPN region through animal studies, there are limited physiological recordings from ambulatory humans. The PPN has recently garnered interest as a potential deep brain stimulation (DBS) target for improving gait and freezing of gait (FoG) in PD. We used bidirectional neurostimulators to record from the human PPN region and GPi in a small cohort of severely affected PD subjects with FoG despite optimized dopaminergic medications. Five subjects, with confirmed on-dopaminergic medication FoG, were implanted with bilateral GPi and bilateral PPN region DBS electrodes. Electrophysiological recordings were obtained during various gait tasks for 5 months postoperatively in both the off- and on-medication conditions (obtained during the no stimulation condition). The results revealed suppression of low beta power in the GPi and a 1–8 Hz modulation in the PPN region which correlated with human gait. The PPN feature correlated with walking speed. GPi beta desynchronization and PPN low-frequency synchronization were observed as subjects progressed from rest to ambulatory tasks. Our findings add to our understanding of the neurophysiology underpinning gait and will likely contribute to the development of novel therapies for abnormal gait in PD. Clinical Trial Registration: Clinicaltrials.gov identifier; NCT02318927. This study aimed to characterize the neurophysiological correlates of gait in the human pedunculopontine nucleus (PPN) region and the globus pallidus internus (GPi) in a Parkinson’s disease (PD) cohort. Though much is known about the PPN region through animal studies, there is limited physiological recordings from ambulatory humans. The PPN has recently garnered interest as a potential deep brain stimulation (DBS) target for improving gait and freezing of gait (FoG) in PD. We used bidirectional neurostimulators to record from the human PPN region and GPi in a small cohort of severely affected PD subjects with FoG despite optimized dopaminergic medications. Five subjects, with confirmed on-dopaminergic medication FoG, were implanted with bilateral GPi and bilateral PPN region DBS electrodes. Electrophysiological recordings were obtained during various gait tasks for five months post-operatively in both the off- and on-medication conditions (obtained during the no stimulation condition). The results revealed suppression of low beta power in the GPi and a 1-8 Hz modulation in the PPN region which correlated with human gait. The PPN feature correlated with walking speed. GPi beta desynchronization and PPN low frequency synchronization was observed as subjects progressed from rest to ambulatory tasks. Our findings add to our understanding of the neurophysiology underpinning gait and will likely contribute to the development of novel therapies for abnormal gait in PD. |
| Author | Sowalsky, Kristen Okun, Michael S. Molina, Rene Hass, Chris J. Martinez-Ramirez, Daniel Foote, Kelly D. Schmitt, Abigail C. Roper, Jaime A. Hess, Christopher W. Opri, Enrico Gunduz, Aysegul |
| AuthorAffiliation | 2 Norman Fixel Institute for Neurological Diseases and the Program for Movement Disorders and Neurorestoration, University of Florida , Gainesville, FL , United States 8 Department of Neurosurgery , University of Florida, Gainesville, FL , United States 3 Department of Applied Physiology and Kinesiology, University of Florida , Gainesville, FL , United States 1 Department of Electrical and Computer Engineering, University of Florida , Gainesville, FL , United States 6 Tecnológico de Monterrey, Escuela de Medicina y Ciencias de la Salud , Monterrey , Mexico 7 Department of Neurology , University of Florida, Gainesville, FL , United States 5 School of Kinesiology, Auburn University , Auburn, AL , United States 4 J. Crayton Pruitt Department of Biomedical Engineering, University of Florida , Gainesville, FL , United States |
| AuthorAffiliation_xml | – name: 1 Department of Electrical and Computer Engineering, University of Florida , Gainesville, FL , United States – name: 4 J. Crayton Pruitt Department of Biomedical Engineering, University of Florida , Gainesville, FL , United States – name: 8 Department of Neurosurgery , University of Florida, Gainesville, FL , United States – name: 3 Department of Applied Physiology and Kinesiology, University of Florida , Gainesville, FL , United States – name: 5 School of Kinesiology, Auburn University , Auburn, AL , United States – name: 2 Norman Fixel Institute for Neurological Diseases and the Program for Movement Disorders and Neurorestoration, University of Florida , Gainesville, FL , United States – name: 6 Tecnológico de Monterrey, Escuela de Medicina y Ciencias de la Salud , Monterrey , Mexico – name: 7 Department of Neurology , University of Florida, Gainesville, FL , United States |
| Author_xml | – sequence: 1 givenname: Rene surname: Molina fullname: Molina, Rene – sequence: 2 givenname: Chris J. surname: Hass fullname: Hass, Chris J. – sequence: 3 givenname: Kristen surname: Sowalsky fullname: Sowalsky, Kristen – sequence: 4 givenname: Abigail C. surname: Schmitt fullname: Schmitt, Abigail C. – sequence: 5 givenname: Enrico surname: Opri fullname: Opri, Enrico – sequence: 6 givenname: Jaime A. surname: Roper fullname: Roper, Jaime A. – sequence: 7 givenname: Daniel surname: Martinez-Ramirez fullname: Martinez-Ramirez, Daniel – sequence: 8 givenname: Christopher W. surname: Hess fullname: Hess, Christopher W. – sequence: 9 givenname: Kelly D. surname: Foote fullname: Foote, Kelly D. – sequence: 10 givenname: Michael S. surname: Okun fullname: Okun, Michael S. – sequence: 11 givenname: Aysegul surname: Gunduz fullname: Gunduz, Aysegul |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32581744$$D View this record in MEDLINE/PubMed |
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| Copyright | Copyright © 2020 Molina, Hass, Sowalsky, Schmitt, Opri, Roper, Martinez-Ramirez, Hess, Foote, Okun and Gunduz. 2020. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Copyright © 2020 Molina, Hass, Sowalsky, Schmitt, Opri, Roper, Martinez-Ramirez, Hess, Foote, Okun and Gunduz. 2020 Molina, Hass, Sowalsky, Schmitt, Opri, Roper, Martinez-Ramirez, Hess, Foote, Okun and Gunduz |
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| Keywords | Parkinson’s disease (PD) brainstem deep brain stimulation (DBS) DBS gait deep brain stimulation |
| Language | English |
| License | Copyright © 2020 Molina, Hass, Sowalsky, Schmitt, Opri, Roper, Martinez-Ramirez, Hess, Foote, Okun and Gunduz. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. cc-by |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 These authors share senior authorship Reviewed by: Chiung-Chu Chen, Linkou Chang Gung Memorial Hospital, Taiwan; Petra Fischer, University of Oxford, United Kingdom Specialty section: This article was submitted to Brain Imaging and Stimulation, a section of the journal Frontiers in Human Neuroscience These authors share first authorship Edited by: Vladimir Litvak, University College London, United Kingdom |
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| SubjectTerms | Basal ganglia brainstem Data collection DBS Deep brain stimulation deep brain stimulation (DBS) Dopamine Dopamine receptors Gait Globus pallidus Human Neuroscience Movement disorders Neurodegenerative diseases Parkinson's disease Parkinson’s disease (PD) Pedunculopontine tegmental nucleus Physiology Signal processing Surgery Synchronization Transplants & implants |
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| Title | Neurophysiological Correlates of Gait in the Human Basal Ganglia and the PPN Region in Parkinson’s Disease |
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