1. Neuroscience

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

  1. Peter M Lauro  Is a corresponding author
  2. Shane Lee
  3. Daniel E Amaya
  4. David D Liu
  5. Umer Akbar
  6. Wael F Asaad  Is a corresponding author
  1. Brown University, United States
  2. Brigham and Women's Hospital, United States
https://doi.org/10.7554/eLife.84135
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  1. Peter M Lauro
  2. Shane Lee
  3. Daniel E Amaya
  4. David D Liu
  5. Umer Akbar
  6. Wael F Asaad
(2023)
Concurrent decoding of distinct neurophysiological fingerprints of tremor and bradykinesia in Parkinson's disease
eLife 12:e84135.
https://doi.org/10.7554/eLife.84135
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Abstract

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.

Data availability

The raw datasets supporting the current study contain patient information and are unique datasets under continued investigation for additional projects, including those of junior trainees.Deidentified neural/behavioral estimates and related code to reproduce all analyses in the manuscript will be made available in a public repository (Dryad; https://doi.org/10.5061/dryad.h9w0vt4n4).To request raw datasets, please contact the corresponding authors (me@peterlauro.me, wael_asaad@brown.edu) with a project proposal. Based upon the granularity of the data requested and potential for patient information exposure, data sharing would granted in consultation with the Lifespan IRB. There are no commercial restrictions for these data currently.

The following data sets were generated

Article and author information

Author details

  1. Peter M Lauro

    Department of Neuroscience, Brown University, Providence, United States
    For correspondence
    me@peterlauro.me
    Competing interests
    Peter M Lauro, The authors have patents and patent applications (US patent #: 17312155, 17470710) broadly relevant to Parkinson's disease (but not directly based upon this work)..
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8569-6427

  2. Shane Lee

    Department of Neuroscience, Brown University, Providence, United States
    Competing interests
    Shane Lee, The authors have patents and patent applications (US patent #: 17312155, 17470710) broadly relevant to Parkinson's disease (but not directly based upon this work)..

  3. Daniel E Amaya

    Department of Neuroscience, Brown University, Providence, United States
    Competing interests
    Daniel E Amaya, The authors have patents and patent applications (US patent #: 17312155, 17470710) broadly relevant to Parkinson's disease (but not directly based upon this work)..

  4. David D Liu

    Department of Neurosurgery, Brigham and Women's Hospital, Boston, United States
    Competing interests
    David D Liu, The authors have patents and patent applications (US patent #: 17312155, 17470710) broadly relevant to Parkinson's disease (but not directly based upon this work)..

  5. Umer Akbar

    Robert J and Nancy D Carney Institute for Brain Science, Brown University, Providence, United States
    Competing interests
    Umer Akbar, The authors have patents and patent applications (US patent #: 17312155, 17470710) broadly relevant to Parkinson's disease (but not directly based upon this work)..

  6. Wael F Asaad

    Department of Neuroscience, Brown University, Providence, United States
    For correspondence
    Wael_Asaad@brown.edu
    Competing interests
    Wael F Asaad, The authors have patents and patent applications (US patent #: 17312155, 17470710) broadly relevant to Parkinson's disease (but not directly based upon this work). WFA has received proprietary equipment and technical support for unrelated research through the Medtronic external research program..
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4406-9096

Funding

National Institute of Neurological Disorders and Stroke (T32MH020068)

  • Peter M Lauro

Doris Duke Charitable Foundation (Clinical Scientist Development Award#2014101)

  • Wael F Asaad

National Institute of General Medical Sciences (P20 GM103645)

  • Wael F Asaad

Neurosurgery Research and Education Foundation

  • Wael F Asaad

Lifespan Norman Prince Neurosciences Institute

  • Shane Lee
  • Umer Akbar
  • Wael F Asaad

Brown University Robert J. and Nancy D. Carney Institute for Brain Science

  • Peter M Lauro
  • Shane Lee
  • Daniel E Amaya
  • Umer Akbar
  • Wael F Asaad

NIH Office of the Director (S10OD025181)

  • Wael F Asaad

Medtronic

  • Wael F Asaad

WFA has received proprietary equipment and technical support for unrelated research through the Medtronic external research program.The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Hayriye Cagnan, University of Oxford, United Kingdom

Ethics

Human subjects: Patients and control subjects agreeing to participate in this study signed informed consent, and experimental procedures were undertaken in accordance with an approved Rhode Island Hospital human research protocol (Lifespan IRB protocol #263157) and the Declaration of Helsinki.

Version history

  1. Preprint posted: February 14, 2022 (view preprint)
  2. Received: October 12, 2022
  3. Accepted: May 26, 2023
  4. Accepted Manuscript published: May 30, 2023 (version 1)
  5. Version of Record published: June 13, 2023 (version 2)

Copyright

© 2023, Lauro et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Peter M Lauro
  2. Shane Lee
  3. Daniel E Amaya
  4. David D Liu
  5. Umer Akbar
  6. Wael F Asaad
(2023)
Concurrent decoding of distinct neurophysiological fingerprints of tremor and bradykinesia in Parkinson's disease
eLife 12:e84135.
https://doi.org/10.7554/eLife.84135

Share this article

https://doi.org/10.7554/eLife.84135

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