Asymmetric neural dynamics characterize loss and recovery of consciousness
Zirui Huang,
Vijay Tarnal,
Phillip E. Vlisides,
Ellen L. Janke,
Amy M. McKinney,
Paul Picton,
George A. Mashour,
Anthony G. Hudetz
Affiliations
Zirui Huang
Department of Anesthesiology, University of Michigan Medical School, Ann Arbor, MI 48109, USA; Center for Consciousness Science, University of Michigan Medical School, Ann Arbor, MI 48109, USA; Corresponding authors.
Vijay Tarnal
Department of Anesthesiology, University of Michigan Medical School, Ann Arbor, MI 48109, USA; Center for Consciousness Science, University of Michigan Medical School, Ann Arbor, MI 48109, USA
Phillip E. Vlisides
Department of Anesthesiology, University of Michigan Medical School, Ann Arbor, MI 48109, USA; Center for Consciousness Science, University of Michigan Medical School, Ann Arbor, MI 48109, USA
Ellen L. Janke
Department of Anesthesiology, University of Michigan Medical School, Ann Arbor, MI 48109, USA; Center for Consciousness Science, University of Michigan Medical School, Ann Arbor, MI 48109, USA
Amy M. McKinney
Department of Anesthesiology, University of Michigan Medical School, Ann Arbor, MI 48109, USA
Paul Picton
Department of Anesthesiology, University of Michigan Medical School, Ann Arbor, MI 48109, USA
George A. Mashour
Department of Anesthesiology, University of Michigan Medical School, Ann Arbor, MI 48109, USA; Center for Consciousness Science, University of Michigan Medical School, Ann Arbor, MI 48109, USA; Neuroscience Graduate Program, University of Michigan, Ann Arbor, MI 48109, USA
Anthony G. Hudetz
Department of Anesthesiology, University of Michigan Medical School, Ann Arbor, MI 48109, USA; Center for Consciousness Science, University of Michigan Medical School, Ann Arbor, MI 48109, USA; Neuroscience Graduate Program, University of Michigan, Ann Arbor, MI 48109, USA; Corresponding authors.
Anesthetics are known to disrupt neural interactions in cortical and subcortical brain circuits. While the effect of anesthetic drugs on consciousness is reversible, the neural mechanism mediating induction and recovery may be different. Insight into these distinct mechanisms can be gained from a systematic comparison of neural dynamics during slow induction of and emergence from anesthesia. To this end, we used functional magnetic resonance imaging (fMRI) data obtained in healthy volunteers before, during, and after the administration of propofol at incrementally adjusted target concentrations. We analyzed functional connectivity of corticocortical and subcorticocortical networks and the temporal autocorrelation of fMRI signal as an index of neural processing timescales. We found that en route to unconsciousness, temporal autocorrelation across the entire brain gradually increased, whereas functional connectivity gradually decreased. In contrast, regaining consciousness was associated with an abrupt restoration of cortical but not subcortical temporal autocorrelation and an abrupt boost of subcorticocortical functional connectivity. Pharmacokinetic effects could not account for the difference in neural dynamics between induction and emergence. We conclude that the induction and recovery phases of anesthesia follow asymmetric neural dynamics. A rapid increase in the speed of cortical neural processing and subcorticocortical neural interactions may be a mechanism that reboots consciousness.