Disrupting abnormal neuronal oscillations with adaptive delayed feedback control

  1. Domingos L Castro
  2. Miguel Aroso
  3. A Pedro Aguiar
  4. David B Grayden
  5. Paulo Aguiar  Is a corresponding author
  1. Universidade do Porto, Portugal
  2. University of Melbourne, Australia

Abstract

Closed-loop neuronal stimulation has a strong therapeutic potential for neurological disorders such as Parkinson's disease. However, at the moment, standard stimulation protocols rely on continuous open-loop stimulation and the design of adaptive controllers is an active field of research. Delayed Feedback Control (DFC), a popular method used to control chaotic systems, has been proposed as a closed-loop technique for desynchronization of neuronal populations but, so far, was only tested in computational studies. We implement DFC for the first time in neuronal populations and access its efficacy in disrupting unwanted neuronal oscillations. To analyse in detail the performance of this activity control algorithm we used specialized in vitro platforms with high spatiotemporal monitoring/stimulating capabilities. We show that the conventional DFC in fact worsens the neuronal population oscillatory behaviour, which was never reported before. Conversely, we present an improved control algorithm, adaptive DFC (aDFC), which monitors the ongoing oscillation periodicity and self-tunes accordingly. aDFC effectively disrupts collective neuronal oscillations restoring a more physiological state. Overall, these results support aDFC as a better candidate for therapeutic closed-loop brain stimulation.

Data availability

The data that support the findings of this study are openly available in ZENODO at the following URL/DOI: https://doi.org/10.5281/zenodo.10138446

The following data sets were generated

Article and author information

Author details

  1. Domingos L Castro

    i3S - Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal
    Competing interests
    The authors declare that no competing interests exist.
  2. Miguel Aroso

    i3S - Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3118-0185
  3. A Pedro Aguiar

    Faculdade de Engenharia, Universidade do Porto, Porto, Portugal
    Competing interests
    The authors declare that no competing interests exist.
  4. David B Grayden

    Department of Biomedical Engineering, University of Melbourne, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
  5. Paulo Aguiar

    i3S - Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal
    For correspondence
    pauloaguiar@i3s.up.pt
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4164-5713

Funding

La Caixa Foundation (HR22-00189)

  • Paulo Aguiar

Santa Casa da Misericórdia de Lisboa (MB-12-2022)

  • Paulo Aguiar

Fundação para a Ciência e a Tecnologia (SFRH/BD/143956/2019)

  • Domingos L Castro

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Brice Bathellier, CNRS, France

Ethics

Animal experimentation: The experiments followed both the European legislation regarding the use of animals for scientific purposes and the protocols approved by the ethical committee of i3S. The Animal Facility of i3S follows the FELASA guidelines and recommendations concerning laboratory animal welfare, complies with the European Guidelines (Directive 2010/63/EU) transposed to Portuguese legislation by Decreto-Lei no 113/2013 and is licensed by the Portuguese official veterinary department (DGAV, Ref 004461).

Version history

  1. Preprint posted: July 6, 2022 (view preprint)
  2. Received: May 5, 2023
  3. Accepted: March 5, 2024
  4. Accepted Manuscript published: March 7, 2024 (version 1)
  5. Version of Record published: April 2, 2024 (version 2)

Copyright

© 2024, Castro 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. Domingos L Castro
  2. Miguel Aroso
  3. A Pedro Aguiar
  4. David B Grayden
  5. Paulo Aguiar
(2024)
Disrupting abnormal neuronal oscillations with adaptive delayed feedback control
eLife 13:e89151.
https://doi.org/10.7554/eLife.89151

Share this article

https://doi.org/10.7554/eLife.89151

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