Abnormal Phase Coupling in Parkinson’s Disease and Normalization Effects of Subthreshold Vestibular Stimulation
The human brain is a highly dynamic structure requiring dynamic coordination between different neural systems to perform numerous cognitive and behavioral tasks. Emerging perspectives on basal ganglia (BG) and thalamic functions have highlighted their role in facilitating and mediating information t...
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| Published in | Frontiers in human neuroscience Vol. 13; p. 118 |
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| Main Authors | , , , |
| Format | Journal Article |
| Language | English |
| Published |
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Frontiers Research Foundation
03.04.2019
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| Abstract | The human brain is a highly dynamic structure requiring dynamic coordination between different neural systems to perform numerous cognitive and behavioral tasks. Emerging perspectives on basal ganglia (BG) and thalamic functions have highlighted their role in facilitating and mediating information transmission among cortical regions. Thus, changes in BG and thalamic structures can induce aberrant modulation of cortico-cortical interactions. Recent work in deep brain stimulation (DBS) has demonstrated that externally applied electrical current to BG structures can have multiple downstream effects in large-scale brain networks. In this work, we identified EEG-based altered resting-state cortical functional connectivity in Parkinson's disease (PD) and examined effects of dopaminergic medication and electrical vestibular stimulation (EVS), a non-invasive brain stimulation (NIBS) technique capable of stimulating the BG and thalamus through vestibular pathways. Resting EEG was collected from 16 PD subjects and 18 age-matched, healthy controls (HC) in four conditions:
(no stimulation), EVS1 (4-8 Hz multisine), EVS2 (50-100 Hz multisine) and EVS3 (100-150 Hz multisine). The mean, variability, and entropy were extracted from time-varying phase locking value (PLV), a non-linear measure of pairwise functional connectivity, to probe abnormal cortical couplings in the PD subjects. We found the mean PLV of Cz and C3 electrodes were important for discrimination between PD and HC subjects. In addition, the PD subjects exhibited lower variability and entropy of PLV (mostly in theta and alpha bands) compared to the controls, which were correlated with their clinical characteristics. While levodopa medication was effective in normalizing the mean PLV only, all EVS stimuli normalized the mean, variability and entropy of PLV in the PD subject, with the exact extent and duration of improvement a function of stimulus type. These findings provide evidence demonstrating both low- and high-frequency EVS exert widespread influences on cortico-cortical connectivity, likely via subcortical activation. The improvement observed in PD in a stimulus-dependent manner suggests that EVS with optimized parameters may provide a new non-invasive means for neuromodulation of functional brain networks. |
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| AbstractList | The human brain is a highly dynamic structure requiring dynamic coordination between different neural systems to perform numerous cognitive and behavioral tasks. Emerging perspectives on basal ganglia (BG) and thalamic functions have highlighted their role in facilitating and mediating information transmission among cortical regions. Thus, changes in BG and thalamic structures can induce aberrant modulation of cortico-cortical interactions. Recent work in deep brain stimulation (DBS) has demonstrated that externally applied electrical current to BG structures can have multiple downstream effects in large-scale brain networks. In this work, we identified EEG-based altered resting-state cortical functional connectivity in Parkinson’s disease (PD) and examined effects of dopaminergic medication and electrical vestibular stimulation (EVS), a non-invasive brain stimulation (NIBS) technique capable of stimulating the BG and thalamus through vestibular pathways. Resting EEG was collected from 16 PD subjects and 18 age-matched, healthy controls (HC) in four conditions:
sham
(no stimulation), EVS1 (4–8 Hz multisine), EVS2 (50–100 Hz multisine) and EVS3 (100–150 Hz multisine). The mean, variability, and entropy were extracted from time-varying phase locking value (PLV), a non-linear measure of pairwise functional connectivity, to probe abnormal cortical couplings in the PD subjects. We found the mean PLV of Cz and C3 electrodes were important for discrimination between PD and HC subjects. In addition, the PD subjects exhibited lower variability and entropy of PLV (mostly in theta and alpha bands) compared to the controls, which were correlated with their clinical characteristics. While levodopa medication was effective in normalizing the mean PLV only, all EVS stimuli normalized the mean, variability and entropy of PLV in the PD subject, with the exact extent and duration of improvement a function of stimulus type. These findings provide evidence demonstrating both low- and high-frequency EVS exert widespread influences on cortico-cortical connectivity, likely via subcortical activation. The improvement observed in PD in a stimulus-dependent manner suggests that EVS with optimized parameters may provide a new non-invasive means for neuromodulation of functional brain networks. The human brain is a highly dynamic structure requiring dynamic coordination between different neural systems to perform numerous cognitive and behavioral tasks. Emerging perspectives on basal ganglia (BG) and thalamic functions have highlighted their role in facilitating and mediating information transmission among cortical regions. Thus, changes in BG and thalamic structures can induce aberrant modulation of cortico-cortical interactions. Recent work in deep brain stimulation (DBS) has demonstrated that externally applied electrical current to BG structures can have multiple downstream effects in large-scale brain networks. In this work, we identified EEG-based altered resting-state cortical functional connectivity in Parkinson's disease (PD) and examined effects of dopaminergic medication and electrical vestibular stimulation (EVS), a non-invasive brain stimulation (NIBS) technique capable of stimulating the BG and thalamus through vestibular pathways. Resting EEG was collected from 16 PD subjects and 18 age-matched, healthy controls (HC) in four conditions: sham (no stimulation), EVS1 (4-8 Hz multisine), EVS2 (50-100 Hz multisine) and EVS3 (100-150 Hz multisine). The mean, variability, and entropy were extracted from time-varying phase locking value (PLV), a non-linear measure of pairwise functional connectivity, to probe abnormal cortical couplings in the PD subjects. We found the mean PLV of Cz and C3 electrodes were important for discrimination between PD and HC subjects. In addition, the PD subjects exhibited lower variability and entropy of PLV (mostly in theta and alpha bands) compared to the controls, which were correlated with their clinical characteristics. While levodopa medication was effective in normalizing the mean PLV only, all EVS stimuli normalized the mean, variability and entropy of PLV in the PD subject, with the exact extent and duration of improvement a function of stimulus type. These findings provide evidence demonstrating both low- and high-frequency EVS exert widespread influences on cortico-cortical connectivity, likely via subcortical activation. The improvement observed in PD in a stimulus-dependent manner suggests that EVS with optimized parameters may provide a new non-invasive means for neuromodulation of functional brain networks.The human brain is a highly dynamic structure requiring dynamic coordination between different neural systems to perform numerous cognitive and behavioral tasks. Emerging perspectives on basal ganglia (BG) and thalamic functions have highlighted their role in facilitating and mediating information transmission among cortical regions. Thus, changes in BG and thalamic structures can induce aberrant modulation of cortico-cortical interactions. Recent work in deep brain stimulation (DBS) has demonstrated that externally applied electrical current to BG structures can have multiple downstream effects in large-scale brain networks. In this work, we identified EEG-based altered resting-state cortical functional connectivity in Parkinson's disease (PD) and examined effects of dopaminergic medication and electrical vestibular stimulation (EVS), a non-invasive brain stimulation (NIBS) technique capable of stimulating the BG and thalamus through vestibular pathways. Resting EEG was collected from 16 PD subjects and 18 age-matched, healthy controls (HC) in four conditions: sham (no stimulation), EVS1 (4-8 Hz multisine), EVS2 (50-100 Hz multisine) and EVS3 (100-150 Hz multisine). The mean, variability, and entropy were extracted from time-varying phase locking value (PLV), a non-linear measure of pairwise functional connectivity, to probe abnormal cortical couplings in the PD subjects. We found the mean PLV of Cz and C3 electrodes were important for discrimination between PD and HC subjects. In addition, the PD subjects exhibited lower variability and entropy of PLV (mostly in theta and alpha bands) compared to the controls, which were correlated with their clinical characteristics. While levodopa medication was effective in normalizing the mean PLV only, all EVS stimuli normalized the mean, variability and entropy of PLV in the PD subject, with the exact extent and duration of improvement a function of stimulus type. These findings provide evidence demonstrating both low- and high-frequency EVS exert widespread influences on cortico-cortical connectivity, likely via subcortical activation. The improvement observed in PD in a stimulus-dependent manner suggests that EVS with optimized parameters may provide a new non-invasive means for neuromodulation of functional brain networks. The human brain is a highly dynamic structure requiring dynamic coordination between different neural systems to perform numerous cognitive and behavioral tasks. Emerging perspectives on basal ganglia (BG) and thalamic functions have highlighted their role in facilitating and mediating information transmission among cortical regions. Thus, changes in BG and thalamic structures can induce aberrant modulation of cortico-cortical interactions. Recent work in deep brain stimulation (DBS) has demonstrated that externally applied electrical current to BG structures can have multiple downstream effects in large-scale brain networks. In this work, we identified EEG-based altered resting-state cortical functional connectivity in Parkinson's disease (PD) and examined effects of dopaminergic medication and electrical vestibular stimulation (EVS), a non-invasive brain stimulation (NIBS) technique capable of stimulating the BG and thalamus through vestibular pathways. Resting EEG was collected from 16 PD subjects and 18 age-matched, healthy controls (HC) in four conditions: (no stimulation), EVS1 (4-8 Hz multisine), EVS2 (50-100 Hz multisine) and EVS3 (100-150 Hz multisine). The mean, variability, and entropy were extracted from time-varying phase locking value (PLV), a non-linear measure of pairwise functional connectivity, to probe abnormal cortical couplings in the PD subjects. We found the mean PLV of Cz and C3 electrodes were important for discrimination between PD and HC subjects. In addition, the PD subjects exhibited lower variability and entropy of PLV (mostly in theta and alpha bands) compared to the controls, which were correlated with their clinical characteristics. While levodopa medication was effective in normalizing the mean PLV only, all EVS stimuli normalized the mean, variability and entropy of PLV in the PD subject, with the exact extent and duration of improvement a function of stimulus type. These findings provide evidence demonstrating both low- and high-frequency EVS exert widespread influences on cortico-cortical connectivity, likely via subcortical activation. The improvement observed in PD in a stimulus-dependent manner suggests that EVS with optimized parameters may provide a new non-invasive means for neuromodulation of functional brain networks. The human brain is a highly dynamic structure requiring dynamic coordination between different neural systems to perform numerous cognitive and behavioural tasks. Emerging perspectives on basal ganglia (BG) and thalamic functions have highlighted their role in facilitating and mediating information transmission among cortical regions. Thus, changes in BG and thalamic structures can induce aberrant modulation of cortico-cortical interactions. Recent work in deep brain stimulation (DBS) has demonstrated that externally applied electrical current to BG structures can have multiple downstream effects in large-scale brain networks. In this work, we identified EEG-based altered resting-state cortical functional connectivity in Parkinson’s disease (PD) and examined effects of dopaminergic medication and electrical vestibular stimulation (EVS), a non-invasive brain stimulation technique capable of stimulating the BG and thalamus through vestibular pathways. Resting EEG was collected from 16 PD subjects and 18 age-matched, healthy controls (HC) in four conditions: sham (no stimulation), EVS1 (4-8 Hz multisine), EVS2 (50-100 Hz multisine) and EVS3 (100-150 Hz multisine). The mean, variability, and entropy were extracted from time-varying phase locking value (PLV), a nonlinear measure of pairwise functional connectivity, to probe abnormal cortical couplings in the PD subjects. We found the mean PLV of Cz and C3 electrodes were important for discrimination between PD and HC subjects. In addition, the PD subjects exhibited lower variability and entropy of PLV (mostly in theta and alpha bands) compared to the controls, which were correlated with their clinical characteristics. While levodopa medication was effective in normalizing the mean PLV only, all EVS stimuli normalized the mean, variability and entropy of PLV in the PD subject, with the exact extent and duration of improvement a function of stimulus type. These findings provide evidence demonstrating both low- and high-frequency EVS exert widespread influences on cortico-cortical connectivity, likely via subcortical activation. The improvement observed in PD in a stimulus-dependent manner suggests that EVS with optimized parameters may provide a new non-invasive means for neuromodulation of functional brain networks. The human brain is a highly dynamic structure requiring dynamic coordination between different neural systems to perform numerous cognitive and behavioral tasks. Emerging perspectives on basal ganglia (BG) and thalamic functions have highlighted their role in facilitating and mediating information transmission among cortical regions. Thus, changes in BG and thalamic structures can induce aberrant modulation of cortico-cortical interactions. Recent work in deep brain stimulation (DBS) has demonstrated that externally applied electrical current to BG structures can have multiple downstream effects in large-scale brain networks. In this work, we identified EEG-based altered resting-state cortical functional connectivity in Parkinson’s disease (PD) and examined effects of dopaminergic medication and electrical vestibular stimulation (EVS), a non-invasive brain stimulation (NIBS) technique capable of stimulating the BG and thalamus through vestibular pathways. Resting EEG was collected from 16 PD subjects and 18 age-matched, healthy controls (HC) in four conditions: sham (no stimulation), EVS1 (4–8 Hz multisine), EVS2 (50–100 Hz multisine) and EVS3 (100–150 Hz multisine). The mean, variability, and entropy were extracted from time-varying phase locking value (PLV), a non-linear measure of pairwise functional connectivity, to probe abnormal cortical couplings in the PD subjects. We found the mean PLV of Cz and C3 electrodes were important for discrimination between PD and HC subjects. In addition, the PD subjects exhibited lower variability and entropy of PLV (mostly in theta and alpha bands) compared to the controls, which were correlated with their clinical characteristics. While levodopa medication was effective in normalizing the mean PLV only, all EVS stimuli normalized the mean, variability and entropy of PLV in the PD subject, with the exact extent and duration of improvement a function of stimulus type. These findings provide evidence demonstrating both low- and high-frequency EVS exert widespread influences on cortico-cortical connectivity, likely via subcortical activation. The improvement observed in PD in a stimulus-dependent manner suggests that EVS with optimized parameters may provide a new non-invasive means for neuromodulation of functional brain networks. |
| Author | Lee, Soojin McKeown, Martin J. Liu, Aiping Wang, Z. Jane |
| AuthorAffiliation | 1 School of Biomedical Engineering, University of British Columbia , Vancouver, BC , Canada 2 Pacific Parkinson’s Research Centre , Vancouver, BC , Canada 5 Department of Medicine (Neurology), University of British Columbia , Vancouver, BC , Canada 3 Department of Electronic Science and Technology, University of Science and Technology of China , Hefei , China 4 Department of Electrical and Computer Engineering, University of British Columbia , Vancouver, BC , Canada |
| AuthorAffiliation_xml | – name: 5 Department of Medicine (Neurology), University of British Columbia , Vancouver, BC , Canada – name: 4 Department of Electrical and Computer Engineering, University of British Columbia , Vancouver, BC , Canada – name: 2 Pacific Parkinson’s Research Centre , Vancouver, BC , Canada – name: 1 School of Biomedical Engineering, University of British Columbia , Vancouver, BC , Canada – name: 3 Department of Electronic Science and Technology, University of Science and Technology of China , Hefei , China |
| Author_xml | – sequence: 1 givenname: Soojin surname: Lee fullname: Lee, Soojin – sequence: 2 givenname: Aiping surname: Liu fullname: Liu, Aiping – sequence: 3 givenname: Z. Jane surname: Wang fullname: Wang, Z. Jane – sequence: 4 givenname: Martin J. surname: McKeown fullname: McKeown, Martin J. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31001099$$D View this record in MEDLINE/PubMed |
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| Copyright | 2019. 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 © 2019 Lee, Liu, Wang and McKeown. 2019 Lee, Liu, Wang and McKeown |
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| Keywords | EEG sample entropy sparse discriminant analysis cortical oscillations phase locking value Parkinson’s disease electrical vestibular stimulation |
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| Snippet | The human brain is a highly dynamic structure requiring dynamic coordination between different neural systems to perform numerous cognitive and behavioral... The human brain is a highly dynamic structure requiring dynamic coordination between different neural systems to perform numerous cognitive and behavioural... |
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| SubjectTerms | Basal ganglia Brain research Cognitive ability Cortex cortical oscillations Deep brain stimulation Dopamine Dopamine receptors EEG electrical vestibular stimulation Electroencephalography Entropy Frequency dependence Information processing Levodopa Movement disorders Neural networks Neurodegenerative diseases Neuromodulation Neuroscience Parkinson's disease phase locking value sample entropy Thalamus Vestibular system |
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| Title | Abnormal Phase Coupling in Parkinson’s Disease and Normalization Effects of Subthreshold Vestibular Stimulation |
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