Global Reduction of Information Exchange during Anesthetic-Induced Unconsciousness

Abstract

During anesthetic-induced unconsciousness (AIU), the brain undergoes a dramatic change in its capacity to exchange information between regions. However, the spatial distribution of information exchange loss/gain across the entire brain remains elusive. In the present study, we acquired and analyzed resting-state functional magnetic resonance imaging (rsfMRI) data in rats during wakefulness and graded levels of consciousness induced by incrementally increasing the concentration of isoflurane. We found that, regardless of spatial scale, the absolute functional connectivity (FC) change was significantly dependent on the FC strength at the awake state across all connections. This dependency became stronger at higher doses of isoflurane. In addition, the relative FC change (i.e. the FC change normalized to the corresponding FC strength at the awake state) exhibited a spatially homogenous reduction across the whole brain particularly after animals lost consciousness, indicating a globally uniform disruption of meaningful information exchange. To further support this notion, we showed that during unconsciousness, the entropy of rsfMRI signal increased to a value comparable to random noise while the mutual information decreased appreciably. Importantly, consistent results were obtained when unconsciousness was induced by dexmedetomidine, an anesthetic agent with a distinct molecular action than isoflurane. This result indicates that the observed global reduction in information exchange may be agent invariant. Taken together, these findings provide compelling neuroimaging evidence suggesting that the brain undergoes a widespread, uniform disruption in the exchange of meaningful information during AIU, and that this change may represent a common systems-level neural mechanism of AIU.