Asymmetric neural dynamics characterize loss and recovery of consciousness

Abstract

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.

Propofol-induced Unresponsiveness Is Associated with a Brain Network Phase Transition

“…This occurs only around the transition to and from unresponsiveness and is a manifestation of the phenomenon of "critical slowing," which is pathognomonic of a phase transition. 25 This is allied with a third indicator, namely hysteresis between losing and regaining consciousness, as has been reported by Huang et al in functional magnetic resonance experiments 37 and by Warnaby et al in clinical studies. 38…”

“…25 This is allied with a third indicator, namely hysteresis between losing and regaining consciousness, as has been reported by Huang et al . in functional magnetic resonance experiments 37 and by Warnaby et al . in clinical studies.…”

Electroencephalographic Evidence for Individual Neural Inertia in Mice That Decreases With Time

“…While we based our upper estimate of the time scale of neural inertia collapse on when we see a behaviorally-derived steady state (McKinstry-Wu et al, 2019;Wasilczuk et al, 2020), this may also not be a safe assumption, and neural inertia could collapse on a timescale longer than several hours. The time course of collapse may additionally vary by species, and may have a role in the variable detection of neural inertia in human studies to date (Warnaby et al, 2017;Colin et al, 2018;Kuizenga et al, 2018;Ferreira et al, 2020;Huang et al, 2021). It is important that we acknowledge we use a measure of net neural activity, EEG spectra, to define neural inertia rather than a behavioral measure, which is how neural inertia was first defined.…”

“…Neural inertia produces a path dependence between induction into and emergence from the anesthetic state, which has been variably observed in humans using behavioral, fMRI, and EEG-derived methods (Warnaby et al, 2017;Kuizenga et al, 2018;Lewis et al, 2018;Ferreira et al, 2020;Huang et al, 2021). Neural inertia has been shown to be subject to genetic control (Joiner et al, 2013), making it a promising avenue for investigation into interindividual variation in anesthetic response.…”

Propofol Anesthesia: A Leap into the Void?

“…Hysteresis has, indeed, been observed in both animals and humans undergoing state transitions and can be attributed to the underlying network dynamics rather than solely to pharmacokinetic factors. [3][4][5][6] As with all studies, this one had technical and analytical limitations, which the authors report clearly. Despite the limitations, the work of Pullon et al 2 prompts further scientific and clinical investigation.…”