Local modulation of human brain responses by circadian rhythmicity and sleep debt.

Human performance is modulated by circadian rhythmicity and homeostatic sleep pressure. Whether and how this interaction is represented at the regional brain level has not been established. We quantified changes in brain responses to a sustained-attention task during 13 functional magnetic resonance imaging sessions scheduled across the circadian cycle, during 42 hours of wakefulness and after recovery sleep, in 33 healthy participants. Cortical responses showed significant circadian rhythmicity, the phase of which varied across brain regions. Cortical responses also significantly decreased with accrued sleep debt. Subcortical areas exhibited primarily a circadian modulation that closely followed the melatonin profile. These findings expand our understanding of the mechanisms involved in maintaining cognition during the day and its deterioration during sleep deprivation and circadian misalignment.

Influence of acute sleep loss on the neural correlates of alerting, orientating and executive attention components.

The Attention Network Test (ANT) is deemed to assess the alerting, orientating and executive components of human attention. Capitalizing on the opportunity to investigate three facets of attention in a single task, we used functional magnetic resonance imaging (fMRI) to assess the effect of sleep deprivation (SD) on brain responses associated with the three attentional components elicited by the ANT. Twelve healthy volunteers were scanned in two conditions 1 week apart, after a normal night of sleep (rested wakefulness, RW) or after one night of total sleep deprivation. Sleep deprivation was associated with a global increase in reaction times, which did not affect specifically any of the three attention effects. Brain responses associated with the alerting effect did not differ between RW and SD. Higher-order attention components (orientating and conflict effects) were associated with significantly larger thalamic responses during SD than during RW. These results suggest that SD influences different components of human attention non-selectively, through mechanisms that might either affect centrencephalic structures maintaining vigilance or ubiquitously perturb neuronal function. Compensatory responses can counter these effects transiently by recruiting thalamic responses, thereby supporting thalamocortical function.

Functional neuroimaging of the reciprocal influences between sleep and wakefulness.

The activity patterns adopted by brain neuronal populations differ dramatically between wakefulness and sleep. However, these vigilance states are not independent and they reciprocally interact. Here, we provide evidence that in humans, regional brain activity during wakefulness is influenced by sleep regulation, namely by the interaction between sleep homeostasis and circadian signals. We also show that, by contrast, regional brain activity during sleep is influenced by the experience acquired during the preceding waking period. These data reveal the dynamic interactions by which the succession of vigilance states support normal brain function and human cognition.

Experience-dependent induction of hypnagogic images during daytime naps: a combined behavioural and EEG study.

This study characterizes hypnagogic hallucinations reported during a polygraphically recorded 90-min daytime nap following or preceding practice of the computer game Tetris. In the experimental group (N = 16), participants played Tetris in the morning for 2 h during three consecutive days, while in a first control group (N = 13, controlling the effect of experience) participants did not play any game, and in a second control group (N = 14, controlling the effect of anticipation) participants played Tetris after the nap. During afternoon naps, participants were repetitively awakened 15, 45, 75, 120 or 180 s after the onset of S1, and were asked to report their mental content. Reports content was scored by three judges (inter-rater reliability 85%). In the experimental group, 48 out of 485 (10%) sleep-onset reports were Tetris-related. They mostly consisted of images and sounds with very little emotional content. They exactly reproduced Tetris elements or mixed them with other mnemonic components. By contrast, in the first control group, only one report out of 107 was scored as Tetris-related (1%), and in the second control group only three reports out of 112 were scored as Tetris-related (3%; between-groups comparison; P = 0.006). Hypnagogic hallucinations were more consistently induced by experience than by anticipation (P = 0.039), and they were predominantly observed during the transition of wakefulness to sleep. The observed attributes of experience-related hypnagogic hallucinations are consistent with the particular organization of regional brain activity at sleep onset, characterized by high activity in sensory cortices and in the default-mode network.