Criticality supports cross-frequency cortical-thalamic information transfer during conscious states
- University of California, Los Angeles, United States
- University of Sydney, Australia
- University of Tokyo, Japan
- Andalusian Center for Molecular Biology and Regenerative Medicine, Spain
- Universitat de Vic-Universitat Central de Catalunya, Spain
- Nagoya City University, Japan
- Institut d'Investigacions biomèdiques de Barcelona, Spain
- 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
Laia Lladó-Pelfort
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.
Reviewing Editor
- Tatyana O Sharpee, Salk Institute for Biological Studies, United States
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.
Version history
- Received: January 31, 2023
- Preprint posted: February 24, 2023 (view preprint)
- Accepted: November 27, 2023
- Accepted Manuscript published: January 5, 2024 (version 1)
- Version of Record published: January 23, 2024 (version 2)
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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Criticality supports cross-frequency cortical-thalamic information transfer during conscious states
eLife 13:e86547.
https://doi.org/10.7554/eLife.86547
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