Department of Neurology, University of California, Los Angeles, Los Angeles, United States; Department of Psychology, University of California, Los Angeles, Los Angeles, United States
Eli Müller
Brain and Mind Centre, University of Sydney, Sydney, Australia
Hiroyuki Miyamoto
Laboratory for Neurogenetics, RIKEN Center for Brain Science, Saitama, Japan; PRESTO, Japan Science and Technology Agency, Saitama, Japan; International Research Center for Neurointelligence, University of Tokyo, Nagoya, Japan
Maurizio S Riga
Andalusian Center for Molecular Biology and Regenerative Medicine, Seville, Spain
Laboratory for Neurogenetics, RIKEN Center for Brain Science, Saitama, Japan; Department of Neurodevelopmental Disorder Genetics, Institute of Brain Science, Nagoya City University Graduate School of Medical Science, Nagoya, Japan
Departament de Neurociències i Terapèutica Experimental, CSIC-Institut d’Investigacions Biomèdiques de Barcelona, Barcelona, Spain; Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Spain; Centro de Investigación Biomédica en Red de Salud Mental (CIBERSAM), Instituto de Salud Carlos III, Madrid, Spain
Brain and Mind Centre, University of Sydney, Sydney, Australia
Andrew E Hudson
Department of Anesthesiology, Veterans Affairs Greater Los Angeles Healthcare System, Los Angeles, United States; Department of Anesthesiology and Perioperative Medicine, University of California, Los Angeles, Los Angeles, United States
Nader Pouratian
Department of Neurological Surgery, UT Southwestern Medical Center, Dallas, United States
Martin M Monti
Department of Psychology, University of California, Los Angeles, Los Angeles, United States; Department of Neurosurgery, University of California, Los Angeles, Los Angeles, United States
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.
