Instability of brain connectivity during nonrapid eye movement sleep reflects altered properties of information integration

Nonrapid eye movement (NREM) sleep is associated with fading consciousness in humans. Recent neuroimaging studies have demonstrated the spatiotemporal alterations of the brain functional connectivity (FC) in NREM sleep, suggesting the changes of information integration in the sleeping brain. However, the common stationarity assumption in FC does not satisfactorily explain the dynamic process of information integration during sleep. The dynamic FC (dFC) across brain networks is speculated to better reflect the time-varying information propagation during sleep. Accordingly, we conducted simultaneous EEG-fMRI recordings involving 12 healthy men during sleep and observed dFC across sleep stages using the sliding-window approach. We divided dFC into two aspects: mean dFC (dFC_mean) and variance dFC (dFC_var). A high dFC_mean indicates stable brain network integrity, whereas a high dFC_var indicates instability of information transfer within and between functional networks. For the network-based dFC, the dFC_var were negatively correlated with the dFC_mean across the waking and three NREM sleep stages. As sleep deepened, the dFC_mean decreased (N0~N1 > N2 > N3), whereas the dFC_var peaked during the N2 stage (N0~N1 < N3 < N2). The highest dFC_var during the N2 stage indicated the unstable synchronizations across the entire brain. In the N3 stage, the overall disrupted network integration was observed through the lowest dFC_mean and elevated dFC_var, compared with N0 and N1. Conclusively, when the network specificity (dFC_mean) breaks down, the consciousness dissipates with increasing variability of information exchange (dFC_var).