Ju Lynn Ong

Cognitive Performance, Sleepiness, and Mood in Partially Sleep Deprived Adolescents: The Need for Sleep Study

STUDY OBJECTIVES To investigate the effects of sleep restriction (7 nights of 5 h time in bed [TIB]) on cognitive performance, subjective sleepiness, and mood in adolescents. METHODS A parallel-group design was adopted in the Need for Sleep Study. Fifty-six healthy adolescents (25 males, age = 15-19 y) who studied in top high schools and were not habitual short sleepers were randomly assigned to Sleep Restriction (SR) or Control groups. Participants underwent a 2-w protocol consisting of 3 baseline nights (TIB = 9 h), 7 nights of sleep opportunity manipulation (TIB = 5 h for the SR and 9 h for the control groups), and 3 nights of recovery sleep (TIB = 9 h) at a boarding school. A cognitive test battery was administered three times each day. RESULTS During the manipulation period, the SR group demonstrated incremental deterioration in sustained attention, working memory and executive function, increase in subjective sleepiness, and decrease in positive mood. Subjective sleepiness and sustained attention did not return to baseline levels even after 2 recovery nights. In contrast, the control group maintained baseline levels of cognitive performance, subjective sleepiness, and mood throughout the study. Incremental improvement in speed of processing, as a result of repeated testing and learning, was observed in the control group but was attenuated in the sleep-restricted participants, who, despite two recovery sleep episodes, continued to perform worse than the control participants. CONCLUSIONS A week of partial sleep deprivation impairs a wide range of cognitive functions, subjective alertness, and mood even in high-performing high school adolescents. Some measures do not recover fully even after 2 nights of recovery sleep. COMMENTARY A commentary on this article appears in this issue on page 497.

Spontaneous eyelid closures link vigilance fluctuation with fMRI dynamic connectivity states

Significance Functionally connected brain networks exhibit recurring connectivity fluctuations. Although such dynamic connectivity states (DCS) can be expected to have behavioral correlates, linking fluctuating connectivity with behavioral state is hampered by the use of mental probes that themselves perturb observed behavior. Using the degree of eyelid closure as a proxy for vigilance state, we were able to continuously assay behavior and constrain the myriad of possible DCS to two relevant states denoting arousal in sleep-deprived persons. Intriguingly, these two DCS had counterparts in task-based data that predicted interindividual differences in the frequency of behavioral lapsing and intraindividual fluctuations in response speed. The replication of these findings in an independent dataset should encourage further investigations into the network dynamics of mental states. Fluctuations in resting-state functional connectivity occur but their behavioral significance remains unclear, largely because correlating behavioral state with dynamic functional connectivity states (DCS) engages probes that disrupt the very behavioral state we seek to observe. Observing spontaneous eyelid closures following sleep deprivation permits nonintrusive arousal monitoring. During periods of low arousal dominated by eyelid closures, sliding-window correlation analysis uncovered a DCS associated with reduced within-network functional connectivity of default mode and dorsal/ventral attention networks, as well as reduced anticorrelation between these networks. Conversely, during periods when participants’ eyelids were wide open, a second DCS was associated with less decoupling between the visual network and higher-order cognitive networks that included dorsal/ventral attention and default mode networks. In subcortical structures, eyelid closures were associated with increased connectivity between the striatum and thalamus with the ventral attention network, and greater anticorrelation with the dorsal attention network. When applied to task-based fMRI data, these two DCS predicted interindividual differences in frequency of behavioral lapsing and intraindividual temporal fluctuations in response speed. These findings with participants who underwent a night of total sleep deprivation were replicated in an independent dataset involving partially sleep-deprived participants. Fluctuations in functional connectivity thus appear to be clearly associated with changes in arousal.

Effects of phase-locked acoustic stimulation during a nap on EEG spectra and declarative memory consolidation.

OBJECTIVES Acoustic stimulation synchronized to slow waves (SWs) can enhance these sleep features and facilitate memory consolidation during nocturnal sleep. Here, we investigated whether a similar benefit could be accrued following stimulation during an afternoon nap. We also evaluated the event-related dynamics of associated EEG spectral changes and their correlation with memory performance. METHODS Sixteen healthy young adults (mean age: 22 ± 1.4 years; nine males) were studied under two conditions: stimulation (STIM) and no stimulation (SHAM), in counter-balanced order. In the STIM condition, acoustic stimulation was delivered using blocks of five tones, each phase-locked to the SW up-state during a 90-min nap opportunity. In the SHAM condition, these time points were marked, but tones were not presented. Prior to the nap, participants learned 40 semantically related word pairs and immediate recall was tested. A delayed recall test was administered 45 min after awakening. RESULTS Compared to the SHAM condition, acoustic stimulation increased SW amplitude, theta, and fast spindle activity and attenuated the forgetting of word pairs (p values < 0.05). CONCLUSION Phase-locked acoustic stimulation can promote sleep-dependent declarative memory during a daytime nap. This can be achieved by stimulation in Stage 2 and SWS without a requirement for high-amplitude slow wave detection.

Co-activated yet disconnected—Neural correlates of eye closures when trying to stay awake

Spontaneous eye-closures that herald sleep onset become more frequent when we are sleep deprived. Although these are typically associated with decreased responsiveness to external stimuli, it is less clear what occurs in the brain at these transitions to drowsiness and light sleep. To investigate this, task-free fMRI of sleep-deprived participants was acquired. BOLD activity associated with periods of spontaneously occurring eye closures were marked and analyzed. We observed concurrent and extensive hypnagogic co-activation of the extrastriate visual, auditory, and somatosensory cortices as well as the default mode network, consistent with internal sensory activity without external stimulation. Co-activation of fronto-parietal areas known to mediate attentional control could correspond with participants resisting sleep or additional engagement of mental imagery. This constellation of signal changes differed from those elicited by cued eye closures of similar duration and distribution in the same, rested participants. They also differ from signal changes associated with mind-wandering and consolidated light sleep. Concurrent with the observed event-related changes, eye closures elicited additional reduction in functional connectivity within nodes of the DMN and DAN, superposed on already reduced connectivity associated with sleep deprivation. There was concurrent deactivation of the thalamus during eye-closure during the sleep-deprived state but almost similar changes occurred in the well-rested state that may also be relevant. These findings highlight the dynamic shifts in brain activity and connectivity at border between wakefulness and sleep.

EEG Changes across Multiple Nights of Sleep Restriction and Recovery in Adolescents: The Need for Sleep Study.

STUDY OBJECTIVES To investigate sleep EEG changes in adolescents across 7 nights of sleep restriction to 5 h time in bed [TIB]) and 3 recovery nights of 9 h TIB. METHODS A parallel-group design, quasi-laboratory study was conducted in a boarding school. Fifty-five healthy adolescents (25 males, age = 15-19 y) who reported habitual TIBs of approximately 6 h on week nights (group average) but extended their sleep on weekends were randomly assigned to Sleep Restriction (SR) or Control groups. Participants underwent a 2-week protocol comprising 3 baseline nights (TIB = 9 h), 7 nights of sleep opportunity manipulation (TIB = 5 h for the SR and 9 h for the Control group), and 3 nights of recovery sleep (TIB = 9 h). Polysomnography was obtained on two baseline, three manipulation, and two recovery nights. RESULTS Across the sleep restriction nights, total SWS duration was preserved relative to the 9 h baseline sleep opportunity, while other sleep stages were reduced. Considering only the first 5 h of sleep opportunity, SR participants had reduced N1 duration and wake after sleep onset (WASO), and increased total sleep time (TST), rapid eye movement (REM) sleep, and slow wave sleep (SWS) relative to baseline. Total REM sleep, N2, and TST duration remained above baseline levels by the third recovery sleep episode. CONCLUSIONS In spite of preservation of SWS duration over multiple nights of sleep restriction, adolescents accustomed to curtailing nocturnal sleep on school day nights evidence residual effects on sleep macro-structure, even after three nights of recovery sleep. Older teenagers may not be as resilient to successive nights of sleep restriction as is commonly believed.

Now You Hear Me, Now You Don't: Eyelid Closures as an Indicator of Auditory Task Disengagement

STUDY OBJECTIVES Eyelid closures in fatigued individuals signify task disengagement in attention-demanding visual tasks. Here, we studied how varying degrees of eyelid closure predict responses to auditory stimuli depending on whether a participant is well rested or sleep deprived. We also examined time-on-task effects and how more and less vulnerable individuals differed in frequency of eye closures and lapses. DESIGN Six repetitions of an auditory vigilance task were performed in each of two sessions: rested wakefulness (RW) and total sleep deprivation (TSD) (order counterbalanced). SETTING Sleep laboratory. PARTICIPANTS Nineteen healthy young adults (mean age: 22 ± 2.8 y; 11 males). INTERVENTION Approximately 24 h of TSD. MEASUREMENTS AND RESULTS Eyelid closure was rated on a 9-point scale (1 = fully closed to 9 = fully opened) using video segments time-locked to the auditory event. Eyes-open trials predominated during RW, but different degrees of eye closure were uniformly distributed during TSD. The frequency of lapses (response time > 800 ms or nonresponses) to auditory stimuli increased dramatically with greater degrees of eye closure, but the association was strong only during TSD. There were significant within-run time-on-task effects on eye closure and auditory lapses that were exacerbated by TSD. Participants who had more auditory lapses during TSD (more vulnerable) had greater variability in their eyelid closures. CONCLUSIONS Eyelid closures are a strong predictor of auditory task disengagement in the sleep-deprived state but are less relevant during rested wakefulness. Individuals relatively more impaired in this auditory vigilance task during total sleep deprivation display oculomotor evidence for greater state instability.

EEG Changes Accompanying Successive Cycles of Sleep Restriction With and Without Naps in Adolescents

Abstract Study objectives: To investigate the temporal evolution of sleep EEG changes in adolescents across two cycles of sleep restriction and recovery simulating an intense school week and to examine the effect of an afternoon nap on nocturnal sleep. Methods: A parallel-group design, quasi-laboratory study was conducted in a student hostel. Fifty-seven adolescents (31 males, age = 15–19 years) were randomly assigned to nap or no nap groups. Participants underwent a 15-day protocol comprising two sleep restriction (5-hour time-in-bed [TIB]) and recovery (9-hour TIB) cycles. The nap group was also provided with a 1-hour nap opportunity at 14:00 following each sleep restriction night. Polysomnography recordings were obtained on nine nights and five nap episodes. Results: Naps reduced homeostatic sleep pressure on sleep restriction nights as evidenced by longer N2 latency and reduced total sleep time (TST), sleep efficiency (SE), and slow wave energy. Sleep debt accumulated in both groups, evidenced by increased TST, greater SE, and reduced wake after sleep onset on recovery compared to baseline nights. Changes were greater in the no nap group. Recovery sleep after the first cycle of sleep restriction did not restore sleep architecture to baseline in either group. SE, rapid eye movement (REM), and non-REM sleep increased, and N2 latency was reduced in the second sleep restriction period. Conclusions: Changes in sleep EEG induced by sleep restriction to 5-hour TIB for five nights were not eliminated after two nights of 9-hour recovery sleep. An afternoon nap helped but residual effects on the sleep EEG suggest that there is no substitute for adequate nocturnal sleep.

Auditory stimulation of sleep slow oscillations modulates subsequent memory encoding through altered hippocampal function

Abstract Study Objectives Slow oscillations (SO) during sleep contribute to the consolidation of learned material. How the encoding of declarative memories during subsequent wakefulness might benefit from their enhancement during sleep is less clear. In this study, we investigated the impact of acoustically enhanced SO during a nap on subsequent encoding of declarative material. Methods Thirty-seven healthy young adults were studied under two conditions: stimulation (STIM) and no stimulation (SHAM), in counter-balanced order following a night of sleep restriction (4 hr time-in-bed [TIB]). In the STIM condition, auditory tones were phase-locked to the SO up-state during a 90 min nap opportunity. In the SHAM condition, corresponding time points were marked but tones were not presented. Thirty minutes after awakening, participants encoded pictures while undergoing fMRI. Picture recognition was tested 60 min later. Results Acoustic stimulation augmented SO across the group, but there was no group level benefit on memory. However, the magnitude of SO enhancement correlated with greater recollection. SO enhancement was also positively correlated with hippocampal activation at encoding. Although spindle activity increased, this did not correlate with memory benefit or shift in hippocampal signal. Conclusions Acoustic stimulation during a nap can benefit encoding of declarative memories. Hippocampal activation positively correlated with SO augmentation.

An end-to-end framework for real-time automatic sleep stage classification

Abstract Sleep staging is a fundamental but time consuming process in any sleep laboratory. To greatly speed up sleep staging without compromising accuracy, we developed a novel framework for performing real-time automatic sleep stage classification. The client–server architecture adopted here provides an end-to-end solution for anonymizing and efficiently transporting polysomnography data from the client to the server and for receiving sleep stages in an interoperable fashion. The framework intelligently partitions the sleep staging task between the client and server in a way that multiple low-end clients can work with one server, and can be deployed both locally as well as over the cloud. The framework was tested on four datasets comprising ≈1700 polysomnography records (≈12000 hr of recordings) collected from adolescents, young, and old adults, involving healthy persons as well as those with medical conditions. We used two independent validation datasets: one comprising patients from a sleep disorders clinic and the other incorporating patients with Parkinson’s disease. Using this system, an entire night’s sleep was staged with an accuracy on par with expert human scorers but much faster (≈5 s compared with 30–60 min). To illustrate the utility of such real-time sleep staging, we used it to facilitate the automatic delivery of acoustic stimuli at targeted phase of slow-sleep oscillations to enhance slow-wave sleep.

Dynamic functional connectivity and its behavioral correlates beyond vigilance.

&NA; Fluctuations in resting‐state functional connectivity and global signal have been found to correspond with vigilance fluctuations, but their associations with other behavioral measures are unclear. We evaluated 52 healthy adolescents after a week of adequate sleep followed by five nights of sleep restriction to unmask inter‐individual differences in cognition and mood. Resting state scans obtained at baseline only, analyzed using sliding window analysis, consistently yielded two polar dynamic functional connectivity states (DCSs) corresponding to previously reported ‘low arousal’ and ‘high arousal’ states. We found that the relative temporal preponderance of two dynamic connectivity states (DCS) in well‐rested participants, indexed by a median split of participants, based on the relative time spent in these DCS, revealed highly significant group differences in vigilance at baseline and its decline following multiple nights of sleep restriction. Group differences in processing speed and working memory following manipulation but not at baseline suggest utility of DCS in predicting cognitive vulnerabilities unmasked by a stressor like sleep restriction. DCS temporal predominance was uninformative about mood and sleepiness speaking to specificity in its behavioral predictions. Global signal fluctuation provided information confined to vigilance. This appears to be related to head motion, which increases during periods of low arousal. Graphical abstract Figure. No caption available. HighlightsTwo polar low & high arousal dynamic connectivity states are observed at baseline.Subjects spent a majority of time in the low arousal state.State dwell times predicted vigilance at baseline and following sleep restriction.Dwell times predicted processing speed & working memory after sleep restriction.Global signal is informative of vigilance; this may be conflated with motion.