Reorganizations of latency structures within the white matter from wakefulness to sleep

Abstract

Previous resting-state functional magnetic resonance imaging (fMRI) studies have revealed highly reproducible latency structures, reflecting the lead/lag relationship of BOLD fMRI signals in white matter (WM). With simultaneous electroencephalography and fMRI data from 35 healthy subjects who were instructed to sleep during imaging, we explored alterations of latency structures in the WM across wakefulness and nonrapid eye movement (NREM) sleep stages. Lagged cross-covariance was computed among voxelwise time series, followed by parabolic interpolation to determine the actual in-between latencies. WM regions, including the brainstem, internal capsule, optic radiation, genu of corpus callosum, and corona radiata, inconsistently changed temporal dynamics with respect to the rest of the WM across wakefulness and NREM sleep stages, as demonstrated when these regions were used as seeds for seed-based latency analysis. Latency analysis of resting-state networks, obtained by applying K-means clustering to a group-level functional connectivity matrix, identified a dominant direction of signaling, starting from the brainstem up to the internal capsule and then the corona radiata during wakefulness, which was reorganized according to stage transitions, e.g., the temporal organization of the internal capsule and corona radiata switched from unidirectional to bidirectional in the wakefulness to N3 transition. These findings suggest that WM BOLD signals are slow, dynamically modulated across wakefulness and NREM sleep stages and that they are involved in maintaining different levels of consciousness.