TY - JOUR
T1 - Criticality supports cross-frequency cortical-thalamic information transfer during conscious states
AU - Toker, Daniel
AU - Müller, Eli
AU - Miyamoto, Hiroyuki
AU - Riga, Maurizio S.
AU - Lladó-Pelfort, Laia
AU - Yamakawa, Kazuhiro
AU - Artigas, Francesc
AU - Shine, James M.
AU - Hudson, Andrew E.
AU - Pouratian, Nader
AU - Monti, Martin M.
N1 - Publisher Copyright:
© 2024, eLife Sciences Publications Ltd. All rights reserved.
PY - 2024
Y1 - 2024
N2 - 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 eluci-dating 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 electrophysi-ology 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.
AB - 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 eluci-dating 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 electrophysi-ology 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.
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U2 - 10.7554/eLife.86547
DO - 10.7554/eLife.86547
M3 - Article
C2 - 38180472
AN - SCOPUS:85183312563
SN - 2050-084X
VL - 13
JO - eLife
JF - eLife
M1 - e86547
ER -