Abstract

Sleepiness and cognitive function vary over the 24-h day due to circadian and sleep-wake-dependent mechanisms. However, the underlying cerebral hallmarks associated with these variations remain to be fully established. Using functional magnetic resonance imaging (fMRI), we investigated brain responses associated with circadian and homeostatic sleep-wake-driven dynamics of subjective sleepiness throughout day and night. Healthy volunteers regularly performed a psychomotor vigilance task (PVT) in the MR-scanner during a 40-h sleep deprivation (high sleep pressure) and a 40-h multiple nap protocol (low sleep pressure). When sleep deprived, arousal-promoting thalamic activation during optimal PVT performance paralleled the time course of subjective sleepiness with peaks at night and troughs on the subsequent day. Conversely, task-related cortical activation decreased when sleepiness increased as a consequence of higher sleep debt. Under low sleep pressure, we did not observe any significant temporal association between PVT-related brain activation and subjective sleepiness. Thus, a circadian modulation in brain correlates of vigilant attention was only detectable under high sleep pressure conditions. Our data indicate that circadian and sleep homeostatic processes impact on vigilant attention via specific mechanisms; mirrored in a decline of cortical resources under high sleep pressure, opposed by a subcortical “rescuing” at adverse circadian times.

Highlights

  • Sleepiness and cognitive function vary over the 24-h day due to circadian and sleep-wake-dependent mechanisms

  • In order to tease the relative contribution of circadian and sleep homeostatic influences on sleepiness apart, vigilant attention and their cerebral correlates was assessed in 31 healthy participants in a balanced cross-over design that comprised a 40-h sleep deprivation (SD) and a 40-h multiple nap protocol (NP)

  • Subjective sleepiness was significantly higher under SD (Mean ± SEM: 5.7 ± 0.16) as compared to NP (Mean ± SEM: 4.3 ± 0.12; main effect of condition; (F (1, 270) = 123.64; p < 0.0001)

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Summary

Introduction

Sleepiness and cognitive function vary over the 24-h day due to circadian and sleep-wake-dependent mechanisms. In order to tease the relative contribution of circadian and sleep homeostatic influences on sleepiness apart, vigilant attention and their cerebral correlates was assessed in 31 healthy participants in a balanced cross-over design that comprised a 40-h SD and a 40-h multiple nap protocol (NP). During both SD and NP, five functional magnetic resonance imaging (fMRI) sessions were individually scheduled at 5, 13, 21, 29, and 37 hours after each individuals’ habitual wake-up time (Fig. 1A). We distinguished between the time course of cerebral correlates underlying slow (>percentile 75) and fast (

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