Cross-Scale Dynamicity of Entropy and Connectivity in the Sleeping Brain

Abstract

Introduction:

The concept of local sleep refers to the phenomenon of local brain activity that modifies neural networks during unresponsive global sleep. Such network rewiring may differ across spatial scales; however, the global and local alterations in brain systems remain elusive in human sleep.

Materials and Methods:

We examined cross-scale changes of brain networks in sleep. Functional magnetic resonance imaging data were acquired from 28 healthy participants during nocturnal sleep. We adopted both metrics of connectivity (functional connectivity [FC] and regional homogeneity [ReHo]) and complexity (multiscale entropy) to explore the global and local functionality of the neural assembly across nonrapid eye movement sleep stages.

Results:

Long-range FC decreased with sleep depth, whereas local ReHo peaked at the N2 stage and reached its lowest level at the N3 stage. Entropy exhibited a general decline at the local scale (Scale 1) as sleep deepened, whereas the coarse-scale entropy (Scale 3) was consistent across stages.

Discussion:

The negative correlation between Scale-1 entropy and ReHo reflects the enhanced signal regularity and synchronization in sleep, identifying the information exchange at the local scale. The N2 stage showed a distinctive pattern toward local information processing with scrambled long-distance information exchange, indicating a specific time window for network reorganization. Collectively, the multidimensional metrics indicated an imbalanced global–local relationship among brain functional networks across sleep–wake stages.

Impact statement

Brain connectivity metrics and multiscale entropy were adopted to examine network-specific patterns throughout the sleep–wake cycle and the local–global balance in brain circuits. The distinct patterns of the cross-scale metrics among sleep-related resting-state networks reflected nonuniform brain activation, supporting the concept of local sleep. The imbalance of global–local relationships reflected by multiscale functional metrics suggests changes in regulation across sleep–wake stages.