Spontaneous neuronal oscillations in the human insula are hierarchically organized traveling waves

  1. Anup Das  Is a corresponding author
  2. John Myers  Is a corresponding author
  3. Raissa Mathura
  4. Ben Shofty
  5. Brian A Metzger
  6. Kelly Bijanki
  7. Chengyuan Wu
  8. Joshua Jacobs  Is a corresponding author
  9. Sameer A Sheth  Is a corresponding author
  1. Columbia University, United States
  2. Baylor College of Medicine, United States
  3. Thomas Jefferson University, United States

Abstract

The insula plays a fundamental role in a wide range of adaptive human behaviors, but its electrophysiological dynamics are poorly understood. Here we used human intracranial electroencephalographic recordings to investigate the electrophysiological properties and hierarchical organization of spontaneous neuronal oscillations within the insula. We analyzed the neuronal oscillations of the insula directly and found that rhythms in the theta and beta frequency oscillations are widespread and spontaneously present. These oscillations are largely organized along the anterior–posterior axis of the insula. Both the left and right insula showed anterior-­to-posterior decreasing gradients for the power of oscillations in the beta frequency band. The left insula also showed a posterior-to-anterior decreasing frequency gradient and an anterior-to-posterior decreasing power gradient in the theta frequency band. In addition to measuring the power of these oscillations, we also examined the phase of these signals across simultaneous recording channels and found that the insula oscillations in the theta and beta bands are traveling waves. The strength of the traveling waves in each frequency was positively correlated with the amplitude of each oscillation. However, the theta and beta traveling waves were uncoupled to each other in terms of phase and amplitude, which suggested that insular traveling waves in the theta and beta bands operate independently. Our findings provide new insights into the spatiotemporal dynamics and hierarchical organization of neuronal oscillations within the insula, which, given its rich connectivity with widespread cortical regions, indicates that oscillations and traveling waves have an important role in intra- and inter-insular communication.

Data availability

Deidentified data are fully available to the public without any restrictions and can be downloaded here https://dabi.loni.usc.edu/dsi/anon?token=Do2yMlnZiXwKwFmOeCDtK. Codes used for the analyses are also fully available to the public without any restrictions and can be downloaded here https://github.com/john-myers-github/INSULA_RS.

The following data sets were generated

Article and author information

Author details

  1. Anup Das

    Department of Biomedical Engineering, Columbia University, New York, United States
    For correspondence
    ad3772@columbia.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8897-7021
  2. John Myers

    Department of Neurosurgery, Baylor College of Medicine, Houston, United States
    For correspondence
    John.Myers@bcm.edu
    Competing interests
    The authors declare that no competing interests exist.
  3. Raissa Mathura

    Department of Neurosurgery, Baylor College of Medicine, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Ben Shofty

    Department of Neurosurgery, Baylor College of Medicine, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Brian A Metzger

    Department of Neurosurgery, Baylor College of Medicine, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Kelly Bijanki

    Department of Neurosurgery, Baylor College of Medicine, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1624-8767
  7. Chengyuan Wu

    Department of Neurosurgery, Thomas Jefferson University, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Joshua Jacobs

    Department of Biomedical Engineering, Columbia University, New York, United States
    For correspondence
    joshua.jacobs@columbia.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1807-6882
  9. Sameer A Sheth

    Department of Neurosurgery, Baylor College of Medicine, Houston, United States
    For correspondence
    Sameer.Sheth@bcm.edu
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institutes of Health (R01-MH127006)

  • Brian A Metzger
  • Kelly Bijanki

National Institutes of Health (K01-MH116364)

  • Brian A Metzger
  • Kelly Bijanki

National Science Foundation (CAREER Award)

  • Joshua Jacobs

McNair Foundation (McNair Foundation)

  • Sameer A Sheth

Dana Foundation (Dana Foundation)

  • Sameer A Sheth

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

Ethics

Human subjects: All decisions regarding the location and coverage of the iEEG probes were based solely on clinical criteria. The Baylor College of Medicine Institutional Review Board approved placement of all electrodes (IRB-18112). All patients provided informed consent before participating.

Copyright

© 2022, Das 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. Anup Das
  2. John Myers
  3. Raissa Mathura
  4. Ben Shofty
  5. Brian A Metzger
  6. Kelly Bijanki
  7. Chengyuan Wu
  8. Joshua Jacobs
  9. Sameer A Sheth
(2022)
Spontaneous neuronal oscillations in the human insula are hierarchically organized traveling waves
eLife 11:e76702.
https://doi.org/10.7554/eLife.76702

Share this article

https://doi.org/10.7554/eLife.76702

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