Brain dynamics exhibit scale-dependent reversibility during consciousness transitions

Abstract

Consciousness is a dynamic brain state, yet the systems-level mechanisms underlying transitions into and out of unconsciousness remain poorly understood. It is unclear whether neural dynamics during loss of consciousness (LOC) and recovery of consciousness (ROC) simply retrace the same trajectory or instead follow distinct paths across multiple spatial scales. Here, we simultaneously measured local electrophysiology, whole-brain functional MRI, and pupil dynamics in rats during graded propofol anesthesia to characterize consciousness transitions from local circuits to whole-brain networks. We found that local field potential, regional BOLD responses, and pairwise functional connectivity exhibited largely reversible changes between LOC and ROC. In contrast, the global brain organization showed distinct and asymmetric patterns during the two transitions, as consistently revealed by traveling-wave propagation, low-dimensional network trajectories, and graph-theoretical analyses. Importantly, brain-wide coupling between pupil dynamics and regional BOLD activity remained highly consistent during LOC and ROC, indicating that these distinct global trajectories cannot be simply explained by differences in neuromodulatory tone. Together, our findings identify scale-dependent reversibility as a systems-level organizing principle of consciousness transitions. These results suggest that recovery of consciousness is an active process of large-scale network reorganization rather than merely the reversal of anesthetic suppression.