Abnormal EEG Spectral Power and Coherence Measures During Pre-Motor Stage in Amyotrophic Lateral Sclerosis
Amyotrophic lateral sclerosis (ALS) is a multisystem neurodegenerative disorder characterized by progressive motor decline. Studies of electroencephalographic (EEG) activity during rest and motor execution have captured network changes in ALS. However, the nature of network-level impairment in the p...
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IEEE
2025-01-01
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| Series: | IEEE Transactions on Neural Systems and Rehabilitation Engineering |
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| Online Access: | https://ieeexplore.ieee.org/document/10816442/ |
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| author | Saroj Bista Amina Coffey Matthew Mitchell Antonio Fasano Stefan Dukic Teresa Buxo Eileen Giglia Mark Heverin Muthuraman Muthuraman Richard G. Carson Madeleine Lowery Lara McManus Orla Hardiman Bahman Nasseroleslami |
| author_facet | Saroj Bista Amina Coffey Matthew Mitchell Antonio Fasano Stefan Dukic Teresa Buxo Eileen Giglia Mark Heverin Muthuraman Muthuraman Richard G. Carson Madeleine Lowery Lara McManus Orla Hardiman Bahman Nasseroleslami |
| author_sort | Saroj Bista |
| collection | DOAJ |
| description | Amyotrophic lateral sclerosis (ALS) is a multisystem neurodegenerative disorder characterized by progressive motor decline. Studies of electroencephalographic (EEG) activity during rest and motor execution have captured network changes in ALS. However, the nature of network-level impairment in the pre-motor activity in ALS remains unclear. Assessing the (dys)function of motor networks engaged prior to motor output is essential for understanding the motor pathophysiology in ALS. We recorded EEG in 22 people with ALS (PwALS) and 16 age-matched healthy controls during rest and isometric pincer-grip tasks. EEG spectral power and coherence were calculated during rest, pre-motor stage, and motor execution. In PwALS, significantly higher event-related spectral perturbations were observed compared to controls over electrodes representing a) contralateral prefrontal and parietal regions in theta band during pre-motor stage, b) contralateral parietal and ipsilateral motor regions in high-beta band during motor execution. Similarly, spectral coherence revealed abnormal EEG connectivity within 1) sensorimotor network during rest in theta band, 2) (pre)motor networks during pre-motor stage in low-alpha and high-beta bands, 3) Fronto-parietal networks during execution in high-beta band. Furthermore, the abnormal EEG connectivity during rest and execution (but not during pre-motor stage) showed significant negative correlation with clinical ALS-functional-rating-scale scores. Combining abnormal EEG connectivity from rest, pre-motor, and execution stages provided more powerful discrimination between patients and controls with a uniquely higher contribution of measures pertaining to the pre-motor stage. The results indicate that pre-motor functional activity reflects a different and unique aspect of network impairment, with potential for inclusion as biomarker candidates in ALS. |
| format | Article |
| id | doaj-art-c9d9e4fc2dbb4436a2959ed3847b91f1 |
| institution | Kabale University |
| issn | 1534-4320 1558-0210 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | IEEE |
| record_format | Article |
| series | IEEE Transactions on Neural Systems and Rehabilitation Engineering |
| spelling | doaj-art-c9d9e4fc2dbb4436a2959ed3847b91f12025-01-08T00:00:16ZengIEEEIEEE Transactions on Neural Systems and Rehabilitation Engineering1534-43201558-02102025-01-013323224210.1109/TNSRE.2024.352310910816442Abnormal EEG Spectral Power and Coherence Measures During Pre-Motor Stage in Amyotrophic Lateral SclerosisSaroj Bista0https://orcid.org/0000-0003-0763-6864Amina Coffey1Matthew Mitchell2Antonio Fasano3https://orcid.org/0000-0002-8727-9141Stefan Dukic4Teresa Buxo5Eileen Giglia6Mark Heverin7Muthuraman Muthuraman8https://orcid.org/0000-0001-6158-2663Richard G. Carson9Madeleine Lowery10https://orcid.org/0000-0001-6743-360XLara McManus11https://orcid.org/0000-0002-2255-7382Orla Hardiman12Bahman Nasseroleslami13https://orcid.org/0000-0002-2227-2176Academic Unit of Neurology, Trinity College Dublin, Dublin 2, IrelandAcademic Unit of Neurology, Trinity College Dublin, Dublin 2, IrelandAcademic Unit of Neurology, Trinity College Dublin, Dublin 2, IrelandAcademic Unit of Neurology, Trinity College Dublin, Dublin 2, IrelandAcademic Unit of Neurology, Trinity College Dublin, Dublin 2, IrelandAcademic Unit of Neurology, Trinity College Dublin, Dublin 2, IrelandAcademic Unit of Neurology, Trinity College Dublin, Dublin 2, IrelandAcademic Unit of Neurology, Trinity College Dublin, Dublin 2, IrelandDepartment of Neurology, University Hospital Würzburg, Würzburg, GermanyTrinity College Institute of Neuroscience and School of Psychology, Trinity College Dublin, Dublin 2, IrelandSchool of Electrical and Electronic Engineering, University College Dublin, Dublin 4, IrelandAcademic Unit of Neurology, Trinity College Dublin, Dublin 2, IrelandAcademic Unit of Neurology, Trinity College Dublin, Dublin 2, IrelandAcademic Unit of Neurology, Trinity College Dublin, Dublin 2, IrelandAmyotrophic lateral sclerosis (ALS) is a multisystem neurodegenerative disorder characterized by progressive motor decline. Studies of electroencephalographic (EEG) activity during rest and motor execution have captured network changes in ALS. However, the nature of network-level impairment in the pre-motor activity in ALS remains unclear. Assessing the (dys)function of motor networks engaged prior to motor output is essential for understanding the motor pathophysiology in ALS. We recorded EEG in 22 people with ALS (PwALS) and 16 age-matched healthy controls during rest and isometric pincer-grip tasks. EEG spectral power and coherence were calculated during rest, pre-motor stage, and motor execution. In PwALS, significantly higher event-related spectral perturbations were observed compared to controls over electrodes representing a) contralateral prefrontal and parietal regions in theta band during pre-motor stage, b) contralateral parietal and ipsilateral motor regions in high-beta band during motor execution. Similarly, spectral coherence revealed abnormal EEG connectivity within 1) sensorimotor network during rest in theta band, 2) (pre)motor networks during pre-motor stage in low-alpha and high-beta bands, 3) Fronto-parietal networks during execution in high-beta band. Furthermore, the abnormal EEG connectivity during rest and execution (but not during pre-motor stage) showed significant negative correlation with clinical ALS-functional-rating-scale scores. Combining abnormal EEG connectivity from rest, pre-motor, and execution stages provided more powerful discrimination between patients and controls with a uniquely higher contribution of measures pertaining to the pre-motor stage. The results indicate that pre-motor functional activity reflects a different and unique aspect of network impairment, with potential for inclusion as biomarker candidates in ALS.https://ieeexplore.ieee.org/document/10816442/Amyotrophic lateral sclerosis (ALS)biomarkersEEG connectivityevent-related spectral perturbationsmotor executionpre-motor |
| spellingShingle | Saroj Bista Amina Coffey Matthew Mitchell Antonio Fasano Stefan Dukic Teresa Buxo Eileen Giglia Mark Heverin Muthuraman Muthuraman Richard G. Carson Madeleine Lowery Lara McManus Orla Hardiman Bahman Nasseroleslami Abnormal EEG Spectral Power and Coherence Measures During Pre-Motor Stage in Amyotrophic Lateral Sclerosis IEEE Transactions on Neural Systems and Rehabilitation Engineering Amyotrophic lateral sclerosis (ALS) biomarkers EEG connectivity event-related spectral perturbations motor execution pre-motor |
| title | Abnormal EEG Spectral Power and Coherence Measures During Pre-Motor Stage in Amyotrophic Lateral Sclerosis |
| title_full | Abnormal EEG Spectral Power and Coherence Measures During Pre-Motor Stage in Amyotrophic Lateral Sclerosis |
| title_fullStr | Abnormal EEG Spectral Power and Coherence Measures During Pre-Motor Stage in Amyotrophic Lateral Sclerosis |
| title_full_unstemmed | Abnormal EEG Spectral Power and Coherence Measures During Pre-Motor Stage in Amyotrophic Lateral Sclerosis |
| title_short | Abnormal EEG Spectral Power and Coherence Measures During Pre-Motor Stage in Amyotrophic Lateral Sclerosis |
| title_sort | abnormal eeg spectral power and coherence measures during pre motor stage in amyotrophic lateral sclerosis |
| topic | Amyotrophic lateral sclerosis (ALS) biomarkers EEG connectivity event-related spectral perturbations motor execution pre-motor |
| url | https://ieeexplore.ieee.org/document/10816442/ |
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