Optogenetics enables real-time spatiotemporal control over spiral wave dynamics in an excitable cardiac system

  1. Rupamanjari Majumder
  2. Iolanda Feola
  3. Alexander S Teplenin
  4. Antoine A F de Vries
  5. Alexander V Panfilov  Is a corresponding author
  6. Daniel A Pijnappels  Is a corresponding author
  1. Leiden University Medical Center, Netherlands
  2. Ghent University, Belgium

Abstract

Propagation of non-linear waves is key to the functioning of diverse biological systems. Such waves can organize into spirals, rotating around a core, whose properties determine the overall wave dynamics. Theoretically, manipulation of a spiral wave core should lead to full spatiotemporal control over its dynamics. However, this theory lacks supportive evidence (even at a conceptual level), making it thus a long-standing hypothesis. Here, we propose a new phenomenological concept that involves artificially dragging spiral waves by their cores, to prove the afore-mentioned hypothesis in silico, with subsequent in vitro validation in optogenetically-modified monolayers of rat atrial cardiomyocytes. We thereby connect previously established, but unrelated concepts of spiral wave attraction, anchoring and unpinning to demonstrate that core manipulation, through controlled displacement of heterogeneities in excitable media, allows forced movement of spiral waves along pre-defined trajectories. Consequently, we impose real-time spatiotemporal control over spiral wave dynamics in a biological system.

Data availability

All data and code generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Rupamanjari Majumder

    Laboratory of Experimental Cardiology, Department of Cardiology, Leiden University Medical Center, Leiden, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  2. Iolanda Feola

    Laboratory of Experimental Cardiology, Department of Cardiology, Leiden University Medical Center, Leiden, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. Alexander S Teplenin

    Laboratory of Experimental Cardiology, Department of Cardiology, Leiden University Medical Center, Leiden, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7841-376X
  4. Antoine A F de Vries

    Laboratory of Experimental Cardiology, Department of Cardiology, Leiden University Medical Center, Leiden, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  5. Alexander V Panfilov

    Department of Physics and Astronomy, Ghent University, Ghent, Belgium
    For correspondence
    Alexander.Panfilov@ugent.be
    Competing interests
    The authors declare that no competing interests exist.
  6. Daniel A Pijnappels

    Laboratory of Experimental Cardiology, Department of Cardiology, Leiden University Medical Center, Leiden, Netherlands
    For correspondence
    D.A.Pijnappels@lumc.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6731-4125

Funding

ZonMw (VIDI)

  • Daniel A Pijnappels

H2020 European Research Council (Starting grant)

  • Daniel A Pijnappels

Ammodo

  • Antoine A F de Vries
  • Daniel A Pijnappels

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

Reviewing Editor

  1. Leon Glass, McGill University, Canada

Ethics

Animal experimentation: All animal experiments were reviewed and approved by the Animal Experiments Committee of the Leiden University Medical Center (AVD 116002017818) and performed in accordance with the recommendations for animal experiments issued by the European Commission directive 2010/63.

Version history

  1. Received: August 13, 2018
  2. Accepted: September 14, 2018
  3. Accepted Manuscript published: September 27, 2018 (version 1)
  4. Version of Record published: October 16, 2018 (version 2)

Copyright

© 2018, Majumder 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. Rupamanjari Majumder
  2. Iolanda Feola
  3. Alexander S Teplenin
  4. Antoine A F de Vries
  5. Alexander V Panfilov
  6. Daniel A Pijnappels
(2018)
Optogenetics enables real-time spatiotemporal control over spiral wave dynamics in an excitable cardiac system
eLife 7:e41076.
https://doi.org/10.7554/eLife.41076

Share this article

https://doi.org/10.7554/eLife.41076

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