Concurrent decoding of distinct neurophysiological fingerprints of tremor and bradykinesia in Parkinson’s disease

Parkinson’s disease (PD) is characterized by distinct motor phenomena that are expressed asynchronously. Understanding the neurophysiological correlates of these motor states could facilitate monitoring of disease progression and allow improved assessments of therapeutic efficacy, as well as enable...

Full description

Bibliographic Details
Main Authors: Peter M Lauro, Shane Lee, Daniel E Amaya, David D Liu, Umer Akbar, Wael F Asaad
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-05-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/84135
_version_ 1797805372723953664
author Peter M Lauro
Shane Lee
Daniel E Amaya
David D Liu
Umer Akbar
Wael F Asaad
author_facet Peter M Lauro
Shane Lee
Daniel E Amaya
David D Liu
Umer Akbar
Wael F Asaad
author_sort Peter M Lauro
collection DOAJ
description Parkinson’s disease (PD) is characterized by distinct motor phenomena that are expressed asynchronously. Understanding the neurophysiological correlates of these motor states could facilitate monitoring of disease progression and allow improved assessments of therapeutic efficacy, as well as enable optimal closed-loop neuromodulation. We examined neural activity in the basal ganglia and cortex of 31 subjects with PD during a quantitative motor task to decode tremor and bradykinesia – two cardinal motor signs of PD – and relatively asymptomatic periods of behavior. Support vector regression analysis of microelectrode and electrocorticography recordings revealed that tremor and bradykinesia had nearly opposite neural signatures, while effective motor control displayed unique, differentiating features. The neurophysiological signatures of these motor states depended on the signal type and location. Cortical decoding generally outperformed subcortical decoding. Within the subthalamic nucleus (STN), tremor and bradykinesia were better decoded from distinct subregions. These results demonstrate how to leverage neurophysiology to more precisely treat PD.
first_indexed 2024-03-13T05:51:05Z
format Article
id doaj.art-a317eaa341dd4c14b5dd2597c2361eb7
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-03-13T05:51:05Z
publishDate 2023-05-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-a317eaa341dd4c14b5dd2597c2361eb72023-06-13T12:50:11ZengeLife Sciences Publications LtdeLife2050-084X2023-05-011210.7554/eLife.84135Concurrent decoding of distinct neurophysiological fingerprints of tremor and bradykinesia in Parkinson’s diseasePeter M Lauro0https://orcid.org/0000-0002-8569-6427Shane Lee1Daniel E Amaya2David D Liu3Umer Akbar4Wael F Asaad5https://orcid.org/0000-0003-4406-9096Department of Neuroscience, Brown University, Providence, United States; Robert J. and Nancy D. Carney Institute for Brain Science, Brown University, Providence, United States; The Warren Alpert Medical School, Brown University, Providence, United StatesDepartment of Neuroscience, Brown University, Providence, United States; Robert J. and Nancy D. Carney Institute for Brain Science, Brown University, Providence, United States; Norman Prince Neurosciences Institute, Rhode Island Hospital, Providence, United States; Department of Neurosurgery, Rhode Island Hospital, Providence, United StatesDepartment of Neuroscience, Brown University, Providence, United States; Robert J. and Nancy D. Carney Institute for Brain Science, Brown University, Providence, United StatesDepartment of Neurosurgery, Brigham and Women’s Hospital, Boston, United StatesRobert J. and Nancy D. Carney Institute for Brain Science, Brown University, Providence, United States; The Warren Alpert Medical School, Brown University, Providence, United States; Norman Prince Neurosciences Institute, Rhode Island Hospital, Providence, United States; Department of Neurology, Rhode Island Hospital, Providence, United StatesDepartment of Neuroscience, Brown University, Providence, United States; Robert J. and Nancy D. Carney Institute for Brain Science, Brown University, Providence, United States; The Warren Alpert Medical School, Brown University, Providence, United States; Norman Prince Neurosciences Institute, Rhode Island Hospital, Providence, United States; Department of Neurosurgery, Rhode Island Hospital, Providence, United StatesParkinson’s disease (PD) is characterized by distinct motor phenomena that are expressed asynchronously. Understanding the neurophysiological correlates of these motor states could facilitate monitoring of disease progression and allow improved assessments of therapeutic efficacy, as well as enable optimal closed-loop neuromodulation. We examined neural activity in the basal ganglia and cortex of 31 subjects with PD during a quantitative motor task to decode tremor and bradykinesia – two cardinal motor signs of PD – and relatively asymptomatic periods of behavior. Support vector regression analysis of microelectrode and electrocorticography recordings revealed that tremor and bradykinesia had nearly opposite neural signatures, while effective motor control displayed unique, differentiating features. The neurophysiological signatures of these motor states depended on the signal type and location. Cortical decoding generally outperformed subcortical decoding. Within the subthalamic nucleus (STN), tremor and bradykinesia were better decoded from distinct subregions. These results demonstrate how to leverage neurophysiology to more precisely treat PD.https://elifesciences.org/articles/84135Parkinson's diseasesubthalamic nucleuselectrocorticographysupport vector regression
spellingShingle Peter M Lauro
Shane Lee
Daniel E Amaya
David D Liu
Umer Akbar
Wael F Asaad
Concurrent decoding of distinct neurophysiological fingerprints of tremor and bradykinesia in Parkinson’s disease
eLife
Parkinson's disease
subthalamic nucleus
electrocorticography
support vector regression
title Concurrent decoding of distinct neurophysiological fingerprints of tremor and bradykinesia in Parkinson’s disease
title_full Concurrent decoding of distinct neurophysiological fingerprints of tremor and bradykinesia in Parkinson’s disease
title_fullStr Concurrent decoding of distinct neurophysiological fingerprints of tremor and bradykinesia in Parkinson’s disease
title_full_unstemmed Concurrent decoding of distinct neurophysiological fingerprints of tremor and bradykinesia in Parkinson’s disease
title_short Concurrent decoding of distinct neurophysiological fingerprints of tremor and bradykinesia in Parkinson’s disease
title_sort concurrent decoding of distinct neurophysiological fingerprints of tremor and bradykinesia in parkinson s disease
topic Parkinson's disease
subthalamic nucleus
electrocorticography
support vector regression
url https://elifesciences.org/articles/84135
work_keys_str_mv AT petermlauro concurrentdecodingofdistinctneurophysiologicalfingerprintsoftremorandbradykinesiainparkinsonsdisease
AT shanelee concurrentdecodingofdistinctneurophysiologicalfingerprintsoftremorandbradykinesiainparkinsonsdisease
AT danieleamaya concurrentdecodingofdistinctneurophysiologicalfingerprintsoftremorandbradykinesiainparkinsonsdisease
AT daviddliu concurrentdecodingofdistinctneurophysiologicalfingerprintsoftremorandbradykinesiainparkinsonsdisease
AT umerakbar concurrentdecodingofdistinctneurophysiologicalfingerprintsoftremorandbradykinesiainparkinsonsdisease
AT waelfasaad concurrentdecodingofdistinctneurophysiologicalfingerprintsoftremorandbradykinesiainparkinsonsdisease