Dynamics of cerebral responses to sustained attention performance during one night of sleep deprivation

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A single night of total sleep deprivation (TSD) can lead to deterioration of multiple aspects of cognition and is associated with disastrous outcomes (Basner et al., 2013; Lim and Dinges, 2010). In an attempt to understand the neural underpinnings of TSD‐related impairment within a specific cognitive domain, most imaging studies of TSD typically conduct two imaging sessions in each subject. One session is performed after rested wakefulness and the other after TSD. By comparing the differences in neural activation between these two sessions, researchers have proposed many explanations, expanding our understanding of the neurocognitive consequences of TSD (Durmer and Dinges, 2005; Goel et al., 2009). However, the observed alterations in neural activation after TSD describe the modulated cerebral responses, rather than the process of modulation. A clearer and more complete understanding of neural changes associated with the process of TSD can be obtained by increasing observation sessions during TSD. This strategy has been used in studying cognitive function recovery from stroke and structural brain changes during normal ageing (Saur et al., 2006; Shaw et al., 2016). Recently, Muto et al. (2016) used 13 functional magnetic resonance imaging (fMRI) sessions during 42 h of TSD and investigated the interaction effect of circadian rhythmicity and sleep debt on brain responses. Their study validated the feasibility and objectivity of repeated measurements of brain activity during TSD. They emphasized the necessity to assess dynamic changes in brain responsiveness during the process of TSD.
Attention is among one of the most severely affected cognitive domains after TSD (Ma et al., 2015). One of the leading tasks probing sustained attention is the psychomotor vigilance task (PVT) (Luquecasado et al., 2016a,b). The fastest reaction times (RTs) (RTs <10th percentile) in the PVT reflect the optimal alertness level. The slowest RTs of PVT (>90th percentile of overall RTs) lengthen dramatically after TSD, reflecting reduced levels of attention and alertness (Lim and Dinges, 2008). Previous studies have indicated that the fastest responses after TSD, and after normal sleep elicited comparable activation in the frontoparietal attention network and motor network, while the slowest RTs were associated with increased covariation within default mode network (DMN) after TSD, which suggested reduced efficiency of task disengagement of the DMN when sleepiness was severely compromised (Drummond et al., 2005). However, how the cerebral responses to fastest RTs and slowest RTs were changed during TSD have not been elucidated clearly.
In the present study, we used repeated fMRI to investigate the dynamic changes in cerebral responses to the fastest and slowest RTs in a PVT during a whole night of TSD. As the dynamic characteristics of cerebral response to TSD might be influenced by the individual differences in chronotype, which refers to individual preference in sleep and wakefulness, only subjects with intermediate chronotype were recruited into our study (Roenneberg et al., 2003). We postulated that, by scanning subjects repeatedly and evenly during TSD, we would be able to identify the dynamic changes in neural responses to a PVT. Specifically, we hypothesized that there are (i) significant differences in PVT activation across the different sessions, both for fastest RTs and slowest RTs; and (ii) cerebral responses for fastest RTs and slowest RTs would show a differential course of activation over time.
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