Erratum: Reconfigurations in brain networks upon awakening from slow wave sleep: Interventions and implications in neural communication.

[This corrects the article DOI: 10.1162/netn_a_00272.].

Reconfigurations in brain networks upon awakening from slow wave sleep: Interventions and implications in neural communication.

Sleep inertia is the brief period of impaired alertness and performance experienced immediately after waking. Little is known about the neural mechanisms underlying this phenomenon. A better understanding of the neural processes during sleep inertia may offer insight into the awakening process. We observed brain activity every 15 min for 1 hr following abrupt awakening from slow wave sleep during the biological night. Using 32-channel electroencephalography, a network science approach, and a within-subject design, we evaluated power, clustering coefficient, and path length across frequency bands under both a control and a polychromatic short-wavelength-enriched light intervention condition. We found that under control conditions, the awakening brain is typified by an immediate reduction in global theta, alpha, and beta power. Simultaneously, we observed a decrease in the clustering coefficient and an increase in path length within the delta band. Exposure to light immediately after awakening ameliorated changes in clustering. Our results suggest that long-range network communication within the brain is crucial to the awakening process and that the brain may prioritize these long-range connections during this transitional state. Our study highlights a novel neurophysiological signature of the awakening brain and provides a potential mechanism by which light improves performance after waking.

Rise and shine: The use of polychromatic short-wavelength-enriched light to mitigate sleep inertia at night following awakening from slow-wave sleep.

Sleep inertia is the brief period of performance impairment and reduced alertness experienced after waking, especially from slow-wave sleep. We assessed the efficacy of polychromatic short-wavelength-enriched light to improve vigilant attention, alertness and mood immediately after waking from slow-wave sleep at night. Twelve participants (six female, 23.3 ± 4.2 years) maintained an actigraphy-confirmed sleep schedule of 8.5 hr for 5 nights, and 5 hr for 1 night prior to an overnight laboratory visit. In the laboratory, participants were awakened from slow-wave sleep, and immediately exposed to either dim, red ambient light (control) or polychromatic short-wavelength-enriched light (light) for 1 hr in a randomized crossover design. They completed a 5-min Psychomotor Vigilance Task, the Karolinska Sleepiness Scale, and Visual Analogue Scales of mood at 2, 17, 32 and 47 min after waking. Following this testing period, lights were turned off and participants returned to sleep. They were awakened from their subsequent slow-wave sleep period and received the opposite condition. Compared with the control condition, participants exposed to light had fewer Psychomotor Vigilance Task lapses (χ2 [1] = 5.285, p = 0.022), reported feeling more alert (Karolinska Sleepiness Scale: F1,77  = 4.955, p = 0.029; Visual Analogue Scalealert : F1,77  = 8.226, p = 0.005), and reported improved mood (Visual Analogue Scalecheerful : F1,77  = 8.615, p = 0.004). There was no significant difference in sleep-onset latency between conditions following the testing period (t10  = 1.024, p = 0.330). Our results suggest that exposure to polychromatic short-wavelength-enriched light immediately after waking from slow-wave sleep at night may help improve vigilant attention, subjective alertness, and mood. Future studies should explore the potential mechanisms of this countermeasure and its efficacy in real-world environments.

Supervision of a self-driving vehicle unmasks latent sleepiness relative to manually controlled driving.

Human error has been implicated as a causal factor in a large proportion of road accidents. Automated driving systems purport to mitigate this risk, but self-driving systems that allow a driver to entirely disengage from the driving task also require the driver to monitor the environment and take control when necessary. Given that sleep loss impairs monitoring performance and there is a high prevalence of sleep deficiency in modern society, we hypothesized that supervising a self-driving vehicle would unmask latent sleepiness compared to manually controlled driving among individuals following their typical sleep schedules. We found that participants felt sleepier, had more involuntary transitions to sleep, had slower reaction times and more attentional failures, and showed substantial modifications in brain synchronization during and following an autonomous drive compared to a manually controlled drive. Our findings suggest that the introduction of partial self-driving capabilities in vehicles has the potential to paradoxically increase accident risk.

Dose-dependent sensorimotor impairment in human ocular tracking after acute low-dose alcohol administration.

KEY POINTS: Oculomotor behaviours are commonly used to evaluate sensorimotor disruption due to ethanol (EtOH). The current study demonstrates the dose-dependent impairment in oculomotor and ocular behaviours across a range of ultra-low BACs (<0.035%). Processing of target speed and direction, as well as pursuit eye movements, are significantly impaired at 0.015% BAC, suggesting impaired neural activity within brain regions associated with the visual processing of motion. Catch-up saccades during steady visual tracking of the moving target compensate for the reduced vigour of smooth eye movements that occurs with the ingestion of low-dose alcohol. Saccade dynamics start to become 'sluggish' at as low as 0.035% BAC. Pupillary light responses appear unaffected at BAC levels up to 0.065%. ABSTRACT: Changes in oculomotor behaviours are often used as metrics of sensorimotor disruption due to ethanol (EtOH); however, previous studies have focused on deficits at blood-alcohol concentrations (BACs) above about 0.04%. We investigated the dose dependence of the impairment in oculomotor and ocular behaviours caused by EtOH administration across a range of ultra-low BACs (≤0.035%). We took repeated measures of oculomotor and ocular performance from sixteen participants, both pre- and post-EtOH administration. To assess the neurological impacts across a wide range of brain areas and pathways, our protocol measured 21 largely independent performance metrics extracted from a range of behavioural responses ranging from ocular tracking of radial step-ramp stimuli, to eccentric gaze holding, to pupillary responses evoked by light flashes. Our results show significant impairment of pursuit and visual motion processing at 0.015% BAC, reflecting degraded neural processing within extrastriate cortical pathways. However, catch-up saccades largely compensate for the tracking displacement shortfall caused by low pursuit gain, although there still is significant residual retinal slip and thus degraded dynamic acuity. Furthermore, although saccades are more frequent, their dynamics are more sluggish (i.e. show lower peak velocities) starting at BAC levels as low as 0.035%. Small effects in eccentric gaze holding and no effect in pupillary response dynamics were observed at levels below 0.07%, showing the higher sensitivity of the pursuit response to very low levels of blood alcohol, under the conditions of our study.

Distinct pattern of oculomotor impairment associated with acute sleep loss and circadian misalignment.

KEY POINTS: Inadequate sleep and irregular work schedules have not only adverse consequences for individual health and well-being, but also enormous economic and safety implications for society as a whole. This study demonstrates that visual motion processing and coordinated eye movements are significantly impaired when performed after sleep loss and during the biological night, and thus may be contributing to human error and accidents. Because affected individuals are often unaware of their sensorimotor and cognitive deficits, there is a critical need for non-invasive, objective indicators of mild, yet potentially unsafe, impairment due to disrupted sleep or biological rhythms. Our findings show that a set of eye-movement measures can be used to provide sensitive and reliable indicators of such mild neural impairments. ABSTRACT: Sleep loss and circadian misalignment have long been known to impair human cognitive and motor performance with significant societal and health consequences. It is well known that human reaction time to a visual cue is impaired following sleep loss and circadian misalignment, but it has remained unclear how more complex visuomotor control behaviour is altered under these conditions. In this study, we measured 14 parameters of the voluntary ocular tracking response of 12 human participants (six females) to systematically examine the effects of sleep loss and circadian misalignment using a constant routine 24-h acute sleep-deprivation paradigm. The combination of state-of-the-art oculometric and sleep-research methodologies allowed us to document, for the first time, large changes in many components of pursuit, saccades and visual motion processing as a function of time awake and circadian phase. Further, we observed a pattern of impairment across our set of oculometric measures that is qualitatively different from that observed previously with other mild neural impairments. We conclude that dynamic vision and visuomotor control exhibit a distinct pattern of impairment linked with time awake and circadian phase. Therefore, a sufficiently broad set of oculometric measures could provide a sensitive and specific behavioural biomarker of acute sleep loss and circadian misalignment. We foresee potential applications of such oculometric biomarkers assisting in the assessment of readiness-to-perform higher risk tasks and in the characterization of sub-clinical neural impairment in the face of a multiplicity of potential risk factors, including disrupted sleep and circadian rhythms.

Validation of a touchscreen psychomotor vigilance task.

OBJECTIVE: The purpose of this study was to compare a psychomotor vigilance task developed for use on touchscreen devices with the original PVT-192 in conditions of acute sleep loss and circadian desynchronization. BACKGROUND: The Psychomotor Vigilance Task (PVT) is considered the gold standard fatigue detection test and is used frequently in fatigue research. With the rapid development of new technologies it is essential to develop a PVT available on different platforms such as touchscreen devices. The advantage of such PVT is that it can be implemented on small devices and can be easily used in field studies. METHODS: Ten participants completed a 5-min PVT (NASA-PVT) on a touchscreen device and a 5-min PVT on the original PVT-192. On the day of the experiment, participants arrived in the lab approximately two hours after their habitual wake time. Participants completed a constant routine protocol under dim lighting, while maintaining a constant posture. The 5-min PVT-192 and NASA-PVT were taken every two hours for at least 24h. RESULTS: The NASA-PVT and PVT-192 were sensitive to extended wakefulness in the same manner. The reaction times were slower and the lapses were higher as time progressed on both NASA-PVT and PVT-192 (p<0.001). Overall, there was a sharp decline in performance after 16h of being awake which coincided with the time the participants were usually going to bed and the worst performance occurred after 24h of wakefulness for both PVTs (p<0.001). CONCLUSIONS: Overall, our data suggest that the NASA-PVT is a valid tool for assessing fatigue in field studies.