Criticality supports cross-frequency cortical-thalamic information transfer during conscious states

  1. Daniel Toker  Is a corresponding author
  2. Eli Müller
  3. Hiroyuki Miyamoto
  4. Maurizio S Riga
  5. Laia Lladó-Pelfort
  6. Kazuhiro Yamakawa
  7. Francesc Artigas
  8. James M Shine
  9. Andrew E Hudson
  10. Nader Pouratian
  11. Martin M Monti
  1. University of California, Los Angeles, United States
  2. University of Sydney, Australia
  3. University of Tokyo, Japan
  4. Andalusian Center for Molecular Biology and Regenerative Medicine, Spain
  5. Universitat de Vic-Universitat Central de Catalunya, Spain
  6. Nagoya City University, Japan
  7. Institut d'Investigacions biomèdiques de Barcelona, Spain
  8. Veterans Affairs Greater Los Angeles Healthcare System, United States

Abstract

Consciousness is thought to be regulated by bidirectional information transfer between the cortex and thalamus, but the nature of this bidirectional communication - and its possible disruption in unconsciousness - remains poorly understood. Here, we present two main findings elucidating mechanisms of corticothalamic information transfer during conscious states. First, we identify a highly preserved spectral channel of cortical-thalamic communication that is present during conscious states, but which is diminished during the loss of consciousness and enhanced during psychedelic states. Specifically, we show that in humans, mice, and rats, information sent from either the cortex or thalamus via 𝛿/𝜃/𝛼 waves (∼1-13 Hz) is consistently encoded by the other brain region by high 𝛾 waves (52-104 Hz); moreover, unconsciousness induced by propofol anesthesia or generalized spike-and-wave seizures diminishes this cross-frequency communication, whereas the psychedelic 5-methoxy-N,N-dimethyltryptamine (5-MeO-DMT) enhances this low-to-high frequency interregional communication. Second, we leverage numerical simulations and neural electrophysiology recordings from the thalamus and cortex of human patients, rats, and mice to show that these changes in cross-frequency cortical-thalamic information transfer may be mediated by excursions of low-frequency thalamocortical electrodynamics toward/away from edge-of-chaos criticality, or the phase transition from stability to chaos. Overall, our findings link thalamic-cortical communication to consciousness, and further offer a novel, mathematically well-defined framework to explain the disruption to thalamic-cortical information transfer during unconscious states.

Data availability

The source data underlying Figures 2-5 and 8-9, and code necessary to run the mean-field simulations of waking, seizure, and anesthesi states are available at https://doi.org/10.6084/m9.figshare.24777081.v2. The raw electrophysiology recordings from Long-Evans rats are available at the Harvard Dataverse Network, with the following DOI: doi:10.7910/DVN/29366.

Article and author information

Author details

  1. Daniel Toker

    Department of Neurology, University of California, Los Angeles, Los Angeles, United States
    For correspondence
    danieltoker@g.ucla.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0983-8937
  2. Eli Müller

    Brain and Mind Centre, University of Sydney, Sydney, Australia
    Competing interests
    The authors declare that no competing interests exist.
  3. Hiroyuki Miyamoto

    6International Research Center for Neurointelligence, University of Tokyo, Nagoya, Japan
    Competing interests
    The authors declare that no competing interests exist.
  4. Maurizio S Riga

    Andalusian Center for Molecular Biology and Regenerative Medicine, Seville, Spain
    Competing interests
    The authors declare that no competing interests exist.
  5. Laia Lladó-Pelfort

    Departament de Ciències Bàsiques, Universitat de Vic-Universitat Central de Catalunya, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1866-5118
  6. Kazuhiro Yamakawa

    Department of Neurodevelopmental Disorder Genetics, Nagoya City University, Nagoya, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1478-4390
  7. Francesc Artigas

    Departament de Neurociències i Terapèutica Experimental, Institut d'Investigacions biomèdiques de Barcelona, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5880-5720
  8. James M Shine

    Brain and Mind Center, University of Sydney, Sydney, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1762-5499
  9. Andrew E Hudson

    Department of Anesthesiology, Veterans Affairs Greater Los Angeles Healthcare System, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Nader Pouratian

    Department of Neurological Surgery, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Martin M Monti

    Department of Neurosurgery, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institutes of Health (5R01GM135420-04)

  • Nader Pouratian

Tiny Blue Dot Foundation (n/a)

  • Martin M Monti

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

Ethics

Animal experimentation: Animal data from previously published studies were re-analyzed in this paper. The following ethics statements are quoted from the relevant papers:GAERS rats (from Miyamoto et al, 2019): "All animal experimental protocols were approved by the Animal Experiment Committee of the RIKEN Center for Brain Science. Mice and rats were handled in accordance with the guidelines of the RIKEN Center for Brain Science Animal Experiment Committee."C57BL/6 mice (from Riga et al 2018): "Animal care followed the European Union regulations (directive 2010/63 of 22/09/2010) and was approved by the Institutional Animal Care and Use Committee."Long-Evans rats (from Reed and Plourde 2015): "This study was carried out in strict accordance with the guidelines of the Canadian Council on Animal Care. The protocol was approved by the Montreal Neurological Institute Animal Care Committee. All surgery was performed under general anesthesia with ketamine and xylazine. All efforts were made to minimize suffering."

Human subjects: Ten subjects with essential tremor undergoing surgery for implantation of deep brain stimulation (DBS) leads in the ventral intermediate nucleus of the thalamus, provided written informed consent according to the Declaration of Helsinki. The institutional review board of the University of California, Los Angeles approved the study protocol.

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. Daniel Toker
  2. Eli Müller
  3. Hiroyuki Miyamoto
  4. Maurizio S Riga
  5. Laia Lladó-Pelfort
  6. Kazuhiro Yamakawa
  7. Francesc Artigas
  8. James M Shine
  9. Andrew E Hudson
  10. Nader Pouratian
  11. Martin M Monti
(2024)
Criticality supports cross-frequency cortical-thalamic information transfer during conscious states
eLife 13:e86547.
https://doi.org/10.7554/eLife.86547

Share this article

https://doi.org/10.7554/eLife.86547

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