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

Consciousness depends on bidirectional communication between the cortex and thalamus. A specific pattern of cross-frequency communication—low-frequency waves (1.5–13 Hz) from one region encoded as high gamma waves (50–100 Hz) in the other—is present during conscious states in humans, mice, and rats. This communication diminishes during propofol-induced anesthesia and generalized spike-and-wave seizures, but is enhanced by the psychedelic 5-MeO-DMT. Numerical simulations and neural recordings show that these changes are mediated by shifts in thalamocortical dynamics toward or away from edge-of-chaos criticality, the phase transition between stability and chaos. The findings offer a mathematically defined framework linking thalamic-cortical communication to consciousness.

Study at a glance

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.