Altered Pallidocortical Low-Beta Oscillations During Self-Initiated Movements in Parkinson Disease
BackgroundParkinson disease (PD) patients have difficulty with self-initiated (SI) movements, presumably related to basal ganglia thalamocortical (BGTC) circuit dysfunction, while showing less impairment with externally cued (EC) movements.ObjectivesWe investigate the role of BGTC in movement initia...
Main Authors: | , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Frontiers Media S.A.
2020-07-01
|
Series: | Frontiers in Systems Neuroscience |
Subjects: | |
Online Access: | https://www.frontiersin.org/article/10.3389/fnsys.2020.00054/full |
_version_ | 1811335646030069760 |
---|---|
author | Jeong Woo Choi Mahsa Malekmohammadi Hiro Sparks Alon Kashanian Katy A. Cross Yvette Bordelon Nader Pouratian Nader Pouratian Nader Pouratian |
author_facet | Jeong Woo Choi Mahsa Malekmohammadi Hiro Sparks Alon Kashanian Katy A. Cross Yvette Bordelon Nader Pouratian Nader Pouratian Nader Pouratian |
author_sort | Jeong Woo Choi |
collection | DOAJ |
description | BackgroundParkinson disease (PD) patients have difficulty with self-initiated (SI) movements, presumably related to basal ganglia thalamocortical (BGTC) circuit dysfunction, while showing less impairment with externally cued (EC) movements.ObjectivesWe investigate the role of BGTC in movement initiation and the neural underpinning of impaired SI compared to EC movements in PD using multifocal intracranial recordings and correlating signals with symptom severity.MethodsWe compared time-resolved neural activities within and between globus pallidus internus (GPi) and motor cortex during between SI and EC movements recorded invasively in 13 PD patients undergoing deep brain stimulation implantation. We compared cortical (but not subcortical) dynamics with those recorded in 10 essential tremor (ET) patients, who do not have impairments in movement initiation.ResultsSI movements in PD are associated with greater low-beta (13–20 Hz) power suppression during pre-movement period in GPi and motor cortex compared to EC movements in PD and compared to SI movements in ET (motor cortex only). SI movements in PD are uniquely associated with significant low-beta pallidocortical coherence suppression during movement execution that correlates with bradykinesia severity. In ET, motor cortex neural dynamics during EC movements do not significantly differ from that observed in PD and do not significantly differ between SI and EC movements.ConclusionThese findings implicate low beta BGTC oscillations in impaired SI movements in PD. These results provide a physiological basis for the strategy of using EC movements in PD, circumventing diseased neural circuits associated with SI movements and instead engaging circuits that function similarly to those without PD. |
first_indexed | 2024-04-13T17:27:20Z |
format | Article |
id | doaj.art-d6e949ce143e46c59523fe12235e1c3d |
institution | Directory Open Access Journal |
issn | 1662-5137 |
language | English |
last_indexed | 2024-04-13T17:27:20Z |
publishDate | 2020-07-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Systems Neuroscience |
spelling | doaj.art-d6e949ce143e46c59523fe12235e1c3d2022-12-22T02:37:44ZengFrontiers Media S.A.Frontiers in Systems Neuroscience1662-51372020-07-011410.3389/fnsys.2020.00054555383Altered Pallidocortical Low-Beta Oscillations During Self-Initiated Movements in Parkinson DiseaseJeong Woo Choi0Mahsa Malekmohammadi1Hiro Sparks2Alon Kashanian3Katy A. Cross4Yvette Bordelon5Nader Pouratian6Nader Pouratian7Nader Pouratian8Department of Neurosurgery, University of California, Los Angeles, Los Angeles, CA, United StatesDepartment of Neurosurgery, University of California, Los Angeles, Los Angeles, CA, United StatesDepartment of Neurosurgery, University of California, Los Angeles, Los Angeles, CA, United StatesDepartment of Neurosurgery, University of California, Los Angeles, Los Angeles, CA, United StatesDepartment of Neurology, University of California, Los Angeles, Los Angeles, CA, United StatesDepartment of Neurology, University of California, Los Angeles, Los Angeles, CA, United StatesDepartment of Neurosurgery, University of California, Los Angeles, Los Angeles, CA, United StatesDepartment of Bioengineering, University of California, Los Angeles, Los Angeles, CA, United StatesBrain Research Institute, University of California, Los Angeles, Los Angeles, CA, United StatesBackgroundParkinson disease (PD) patients have difficulty with self-initiated (SI) movements, presumably related to basal ganglia thalamocortical (BGTC) circuit dysfunction, while showing less impairment with externally cued (EC) movements.ObjectivesWe investigate the role of BGTC in movement initiation and the neural underpinning of impaired SI compared to EC movements in PD using multifocal intracranial recordings and correlating signals with symptom severity.MethodsWe compared time-resolved neural activities within and between globus pallidus internus (GPi) and motor cortex during between SI and EC movements recorded invasively in 13 PD patients undergoing deep brain stimulation implantation. We compared cortical (but not subcortical) dynamics with those recorded in 10 essential tremor (ET) patients, who do not have impairments in movement initiation.ResultsSI movements in PD are associated with greater low-beta (13–20 Hz) power suppression during pre-movement period in GPi and motor cortex compared to EC movements in PD and compared to SI movements in ET (motor cortex only). SI movements in PD are uniquely associated with significant low-beta pallidocortical coherence suppression during movement execution that correlates with bradykinesia severity. In ET, motor cortex neural dynamics during EC movements do not significantly differ from that observed in PD and do not significantly differ between SI and EC movements.ConclusionThese findings implicate low beta BGTC oscillations in impaired SI movements in PD. These results provide a physiological basis for the strategy of using EC movements in PD, circumventing diseased neural circuits associated with SI movements and instead engaging circuits that function similarly to those without PD.https://www.frontiersin.org/article/10.3389/fnsys.2020.00054/fullParkinson diseaseself-initiated movementsbasal ganglia thalamocortical networklocal field potentialbeta oscillations |
spellingShingle | Jeong Woo Choi Mahsa Malekmohammadi Hiro Sparks Alon Kashanian Katy A. Cross Yvette Bordelon Nader Pouratian Nader Pouratian Nader Pouratian Altered Pallidocortical Low-Beta Oscillations During Self-Initiated Movements in Parkinson Disease Frontiers in Systems Neuroscience Parkinson disease self-initiated movements basal ganglia thalamocortical network local field potential beta oscillations |
title | Altered Pallidocortical Low-Beta Oscillations During Self-Initiated Movements in Parkinson Disease |
title_full | Altered Pallidocortical Low-Beta Oscillations During Self-Initiated Movements in Parkinson Disease |
title_fullStr | Altered Pallidocortical Low-Beta Oscillations During Self-Initiated Movements in Parkinson Disease |
title_full_unstemmed | Altered Pallidocortical Low-Beta Oscillations During Self-Initiated Movements in Parkinson Disease |
title_short | Altered Pallidocortical Low-Beta Oscillations During Self-Initiated Movements in Parkinson Disease |
title_sort | altered pallidocortical low beta oscillations during self initiated movements in parkinson disease |
topic | Parkinson disease self-initiated movements basal ganglia thalamocortical network local field potential beta oscillations |
url | https://www.frontiersin.org/article/10.3389/fnsys.2020.00054/full |
work_keys_str_mv | AT jeongwoochoi alteredpallidocorticallowbetaoscillationsduringselfinitiatedmovementsinparkinsondisease AT mahsamalekmohammadi alteredpallidocorticallowbetaoscillationsduringselfinitiatedmovementsinparkinsondisease AT hirosparks alteredpallidocorticallowbetaoscillationsduringselfinitiatedmovementsinparkinsondisease AT alonkashanian alteredpallidocorticallowbetaoscillationsduringselfinitiatedmovementsinparkinsondisease AT katyacross alteredpallidocorticallowbetaoscillationsduringselfinitiatedmovementsinparkinsondisease AT yvettebordelon alteredpallidocorticallowbetaoscillationsduringselfinitiatedmovementsinparkinsondisease AT naderpouratian alteredpallidocorticallowbetaoscillationsduringselfinitiatedmovementsinparkinsondisease AT naderpouratian alteredpallidocorticallowbetaoscillationsduringselfinitiatedmovementsinparkinsondisease AT naderpouratian alteredpallidocorticallowbetaoscillationsduringselfinitiatedmovementsinparkinsondisease |