Cortical network functional connectivity in the descent to sleep

Abstract

Descent into sleep is accompanied by disengagement of the conscious brain from the external world. It follows that this process should be associated with reduced neural activity in regions of the brain known to mediate interaction with the environment. We examined blood oxygen dependent (BOLD) signal functional connectivity using conventional seed-based analyses in 3 primary sensory and 3 association networks as normal young adults transitioned from wakefulness to light sleep while lying immobile in the bore of a magnetic resonance imaging scanner. Functional connectivity was maintained in each network throughout all examined states of arousal. Indeed, correlations within the dorsal attention network modestly but significantly increased during light sleep compared to wakefulness. Moreover, our data suggest that neuronally mediated BOLD signal variance generally increases in light sleep. These results do not support the view that ongoing BOLD fluctuations primarily reflect unconstrained cognition. Rather, accumulating evidence supports the hypothesis that spontaneous BOLD fluctuations reflect processes that maintain the integrity of functional systems in the brain.

Fig. 1.

Conjunction analysis of cognitive network seed correlations in wake (i) and light NREM sleep (ii). Seed ROIs are indicated by open circles (i) in all cases. There is wide-spread correspondence in the principal ROIs for each network across subjects (n = 6), and network connectivity is maintained in sleep for all networks.

Fig. 2.

Conjunction analysis of cross-hemispheric connectivity in sensory systems showing that connections are maintained in light NREM sleep. Seed regions (open circles) were created in the left sensory cortex (see Table 1) and show strong cross-hemispheric connectivity across all subjects (n = 6) in wake (i) that is maintained in sleep (ii).

Fig. 3.

BOLD signal variance was examined in the regressed whole brain signal (Ai, whole brain) and in each distributed network ROI following all regressions steps (Aii, solid bars). Whole brain signal variance showed a statistically significant increase with descent to sleep. There was a general trend toward increased signal variance in sleep (blue) relative to wake (red) in individual ROIs although this did not reach statistical significance. (B) A visual representation of the change in signal variance across state is illustrated. BOLD timecourses for each ROI in the default network are shown overlaid in the transition from wake (red) to sleep (blue). (C) Analysis of the BOLD spectral content demonstrates a general trend toward lower frequency bins in sleep (dashed lines) that was not statistically significant using either parametric (T, P > 0.14, SE50, P > 0.18, SE90, n = 6 per network) or nonparametric (Wilcoxon rank sum, P > 0.44 SE50, P > 0.30 SE90, n = 6 per network) methods.