Criticality supports cross-frequency cortical-thalamic information transfer during conscious states
Daniel Toker, Eli Müller, Hiroyuki Miyamoto, Maurizio S. Riga, Laia Lladó-Pelfort, Kazuhiro Yamakawa, Francesc Artigas, James M. Shine, Andrew E. Hudson, Nader Pouratian, Martin M. Monti
bioRxiv Preprint Server February 22, 2023 preprint DOI: 10.1101/2023.02.22.529544 via bioRxiv
Summary
The study identifies a preserved channel of communication between the cortex and thalamus that is active during consciousness but weakened during unconsciousness. Specifically, the transfer of information through δ/θ/α waves (1.5-13 Hz) is diminished under propofol anesthesia or seizures, while enhanced by the psychedelic 5-MeO-DMT. The findings suggest that changes in this communication are linked to transitions between stability and chaos in brain activity, providing insights into how consciousness may be regulated.
Study at a glance
| Population | humans, mice, and rats |
|---|---|
| Key finding | Corticothalamic communication is diminished during unconsciousness and enhanced during psychedelic states, linked to changes in brain wave patterns. |
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 which 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 (~1.5-13 Hz) is consistently encoded by the other brain region by high γ waves (~50-100 Hz); moroever, 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 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 are 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.