Analysis of postarousal EEG activity during somnambulistic episodes

Early studies found that electroencephalographic (EEG) recordings during somnambulistic episodes were characterized by a combination of alpha, theta, and delta frequencies, without evidence of clear wakefulness. Three postarousal EEG patterns associated with slow-wave sleep (SWS) arousals were recently identified in adults with sleepwalking and sleep terrors. The goal of the present study was to evaluate the distribution of these postarousal EEG patterns in 10 somnambulistic patients (three males, seven females, mean age: 25.1, SD: 4.1) evaluated at baseline and following 38 h of sleep deprivation. A total of 44 behavioral arousals were recorded in the laboratory; seven episodes at baseline (five from SWS, two from stage 2 sleep) and 37 episodes during recovery sleep (30 from SWS, seven from stage 2 sleep). There was no significant difference in the distribution of postarousal EEG patterns identified during baseline and recovery sleep. One pattern, comprised of diffuse rhythmic and synchronous delta activity, was preferentially associated with relatively simple behavioral episodes but did not occur during episodes from stage 2 sleep. Overall, delta activity was detected in 48% of the behavioral episodes from SWS and in 22% of those from stage 2. There was no evidence of complete awakening during any of the episodes. The results support the view of somnambulism as a disorder of arousal and suggest that sleepwalkers' atypical arousal reactions can manifest themselves in stage 2 sleep in addition to SWS.     

Relationships between affect, vigilance, and sleepiness following sleep deprivation

This pilot study examined the relationships between the effects of sleep deprivation on subjective and objective measures of sleepiness and affect, and psychomotor vigilance performance. Following an adaptation night in the laboratory, healthy young adults were randomly assigned to either a night of total sleep deprivation (SD group; n = 15) or to a night of normal sleep (non-SD group; n = 14) under controlled laboratory conditions. The following day, subjective reports of mood and sleepiness, objective sleepiness (Multiple Sleep Latency Test and spontaneous oscillations in pupil diameter, PUI), affective reactivity/regulation (pupil dilation responses to emotional pictures), and psychomotor vigilance performance (PVT) were measured. Sleep deprivation had a significant impact on all three domains (affect, sleepiness, and vigilance), with significant group differences for eight of the nine outcome measures. Exploratory factor analyses performed across the entire sample and within the SD group alone revealed that the outcomes clustered on three orthogonal dimensions reflecting the method of measurement: physiological measures of sleepiness and affective reactivity/regulation, subjective measures of sleepiness and mood, and vigilance performance. Sleepiness and affective responses to sleep deprivation were associated (although separately for objective and subjective measures). PVT performance was also independent of the sleepiness and affect outcomes. These findings suggest that objective and subjective measures represent distinct entities that should not be assumed to be equivalent. By including affective outcomes in experimental sleep deprivation research, the impact of sleep loss on affective function and their relationship to other neurobehavioral domains can be assessed.     

Sleep deprivation impairs long-term potentiation in rat hippocampal slices

To determine if 12-h sleep deprivation disrupts neural plasticity, we compared long-term potentiation (LTP) in five sleep-deprived and five control rats. Thirty minutes after tetanus population spike amplitude increased 101 +/- 15% in 16 slices from sleep deprived rats and 139 +/- 14% in 14 slices from control rats. This significant (P < 0.05) reduction of LTP, the first demonstration that the sleep deprivation protocol impairs plasticity in adult rats, may be due to several factors. Reduced LTP may indicate that sleep provides a period of recuperation for cellular processes underlying neural plasticity. Alternatively, the stress of sleep deprivation, as indicated by elevated blood corticosterone levels, or other non-sleep-specific factors of deprivation may contribute to the LTP reduction.     

The effects of chewing versus caffeine on alertness, cognitive performance and cardiac autonomic activity during sleep deprivation

Chewing has been shown to alleviate feelings of sleepiness and improve cognitive performance during the day. This study investigated the effect of chewing on alertness and cognitive performance across one night without sleep as well as the possible mediating role of cardiac autonomic activity. Fourteen adults participated in a randomized, counterbalanced protocol employing a chewing, placebo and caffeine condition. Participants completed tasks assessing psychomotor vigilance, tracking, grammatical reasoning, alertness and sleepiness each hour across the night. All participants received either placebo or caffeine (200 mg), while the chewing condition also chewed on a tasteless and odorless substance for 15 min each hour. Heart rate (HR), root mean square of the successive differences in R-R intervals on the ECG (RMSSD), and preejection period (PEP) were simultaneously recorded. Alertness and cognitive performance amongst the chewing condition did not differ or were in fact worse when compared with placebo. Similarly, measures of HR and RMSSD remained the same between these two conditions; however, PEP was reduced in the later part of the night in the chewing condition compared with a relative increase for placebo. Caffeine led to improved speed and accuracy on cognitive tasks and increased alertness when compared with chewing. Relative increases in RMSSD and reductions in HR were demonstrated following caffeine; however, no change in PEP was seen. Strong associations between cardiac parasympathetic activity and complex cognitive tasks, as well as between subjective alertness and simpler cognitive tasks, suggest a differential process mediating complex versus simple cognitive performance during sleep deprivation.     

Sleep deprivation impairs binding of information with its context

Binding information to its context in long-term memory is critical for many tasks, including memory tasks and decision making. Failure to associate information to its context could be an important aspect of sleep deprivation effects on cognition, but little is known about binding problems from being sleep-deprived at the time of encoding. We studied how sleep deprivation affects binding using a well-established paradigm testing the ability to remember auditorily presented words (items) and their speakers (source context). In a laboratory study, 68 healthy young adults were randomly assigned to total sleep deprivation or a well-rested control condition. Participants completed an affective item and source memory task twice: once after 7-hour awake during baseline and again 24 hours later, after nearly 31 hours awake in the total sleep deprivation condition or 7 hours awake in the control condition. Participants listened to negative, positive, and neutral words presented by a male or female speaker and were immediately tested for recognition of the words and their respective speakers. Recognition of items declined during sleep deprivation, but even when items were recognized accurately, recognition of their associated sources also declined. Negative items were less bound with their sources than positive or neutral items, but sleep deprivation did not significantly affect this pattern. Our findings indicate that learning while sleep-deprived disrupts the binding of information to its context independent of item valence. Such binding failures may contribute to sleep deprivation effects on tasks requiring the ability to bind new information together in memory.     

Sleep restriction for the duration of a work week impairs multitasking performance

It is important to develop shift schedules that minimise the chance for sleep‐related human error in safety‐critical domains. Experimental data on the effects of sleep restriction (SR) play a key role in this development work. In order to provide such data, we conducted an experiment in which cognitively demanding and long‐duration task performance, simulating task performance at work, was measured under SR and following recovery. Twenty healthy male volunteers, aged 19–29 years, participated in the study. Thirteen of them had first two baseline days (8‐h sleep opportunity per day), then five SR days (4‐h sleep) and finally two recovery days (8‐h sleep). Seven controls were allowed to sleep for 8 h each night. On each experimental day, multitask performance was tested in 50‐min sessions, physiological sleepiness was evaluated during multitask performance using electroencephalogram (EEG)/electrooculogram (EOG) recordings, and psychomotor vigilance task performance and Karolinska Sleepiness Scale were recorded. Sleep–wake rhythm was monitored throughout the experiment. The multitask performance progressively deteriorated as a result of prolongation of the SR and the time spent on the task. The effect was significant at group level, but individual differences were large: performance was not markedly deteriorated in all participants. Similar changes were observed also in EEG/EOG‐defined sleepiness. The recovery process of performance and sleepiness from the SR continued over the two recovery sleep opportunities. In all, our findings emphasise the importance of shift systems that do not restrict sleep for several consecutive days.     

Sleep complaints and risk factors for excessive daytime sleepiness in adult males in Northern Ireland

The prevalence of sleep complaints in Northern Ireland is unknown. Sleep disruption can result in excessive daytime sleepiness (EDS), with significant socioeconomic consequences. The aim of this study was to assess the prevalence of sleep complaints and to determine risk factors for EDS in a Northern Irish community. From an urban and rural community of 499,111 people, a random sample of 3391 adult men were sent a questionnaire by mail. Questions were asked regarding sleep, EDS and medical history. There were 2364 completed questionnaires returned (response rate 70%). The mean age of respondents was 46.0 years (range 18--91 years). 26.7% of men were not satisfied with their usual night's sleep and 68% of men woke up at least once during the night. Based on pre-defined criteria, 24.6% of the population had insomnia and 19.8% had EDS. The strongest risk factor identified for EDS was a history of snoring loudly (odds ratio 2.62; 95% CI 1.82--3.77). Other risk factors included ankle swelling, feeling sad or depressed stopping sleep, experiencing vivid dreams while falling asleep, waking up feeling unrefreshed and age > 35 years. The prevalence rates of sleep complaints and EDS in this community-based study is high, although this does depend directly on the criteria used to define insomnia and EDS. Recognition of risk factors for EDS may help to identify and treat those affected.     

Sleep deprivation impairs spatial working memory and reduces hippocampal AMPA receptor phosphorylation

Sleep is important for brain function and cognitive performance. Sleep deprivation (SD) may affect subsequent learning capacity and ability to form new memories, particularly in the case of hippocampus‐dependent tasks. In the present study we examined whether SD for 6 or 12 h during the normal resting phase prior to learning affects hippocampus‐dependent working memory in mice. In addition, we determined effects of SD on hippocampal glutamate α‐amino‐3‐hydroxy‐5‐methyl‐4‐isoxazolepropionic acid (AMPA) receptors and their regulatory pathways, which are crucially involved in working memory. After 12 h SD, but not yet after 6 h, spatial working memory in a novel arm recognition task was significantly impaired. This deficit was not likely due to stress as corticosterone levels after SD were not significantly different between groups. In parallel with the change in cognitive function, we found that 12 h SD significantly reduced hippocampal AMPA receptor phosphorylation at the GluR1‐S845 site, which is important for incorporation of the receptors into the membrane. SD did not affect protein levels of cyclic‐AMP‐dependent protein kinase A (PKA) or phosphatase calcineurin (CaN), which regulate GluR1 phosphorylation. However, SD did reduce the expression of the scaffolding molecule A‐kinase anchoring protein 150 (AKAP150), which binds and partly controls the actions of PKA and CaN. In conclusion, a relatively short SD during the normal resting phase may affect spatial working memory in mice by reducing hippocampal AMPA receptor function through a change in AKAP150 levels. Together, these findings provide further insight into the possible mechanism of SD‐induced hippocampal dysfunction and memory impairment.     

Sleep condition and cognitive decline in Japanese community‐dwelling older people: Data from a 4‐year longitudinal study

This study examined whether sleep duration and excessive daytime sleepiness (EDS) are related to cognitive decline among community‐dwelling older adults with intact cognition at baseline, using 4‐year longitudinal data. A total of 3,151 community‐dwelling older individuals aged ≥65 years were studied. They were assessed for cognitive function, including memory, attention, executive function and processing speed. Cognitive impairment was defined based on a score >1.5 standard deviations below the age‐ and education‐specific mean. Cognitive decline was defined in one or more cognitive tests at follow‐up. Self‐reported sleep duration (short, ≤6.0 hr; medium, 6.1–8.9 hr; long, ≥9.0 hr) and EDS at first‐wave examination were assessed and logistic regression analyses were used to examine the associations of sleep duration and EDS with cognitive status at second‐wave examination. The incidence of cognitive decline differed significantly among the sleep‐duration groups (short, 15.9%; medium, 11.9%; long, 20.1%; p = 0.001). The prevalence of having EDS was 13.1%, which was associated with a higher rate of cognitive decline than having no EDS (18.9% vs. 12.5%, p = 0.004). Long sleep duration compared with medium sleep duration (OR, 1.50; 95% CI, 1.05–2.13) and EDS (1.43; 1.01–2.03) independently impacted the incidence of cognitive decline. The results were similar after multiple imputations (long, 1.68, 1.12–2.52; EDS, 1.55, 1.05–2.29). In conclusion, our study revealed that both long sleep duration and EDS were independent risk factors associated with cognitive decline after 4 years among older adults.     

Improved vigilance after sodium oxybate treatment in narcolepsy: a comparison between in‐field and in‐laboratory measurements

This two‐centre observational study of vigilance measurements assessed the feasibility of vigilance measurements on multiple days using the Sustained Attention to Response Task and the Psychomotor Vigilance Test with portable task equipment, and subsequently assessed the effect of sodium oxybate treatment on vigilance in patients with narcolepsy. Twenty‐six patients with narcolepsy and 15 healthy controls were included. The study comprised two in‐laboratory days for the Maintenance of Wakefulness Test and the Oxford Sleep Resistance test, followed by 7‐day portable vigilance battery measurements. This procedure was repeated for patients with narcolepsy after at least 3 months of stable treatment with sodium oxybate. Patients with narcolepsy had a higher Sustained Attention to Response Task error count, lower Psychomotor Vigilance Test reciprocal reaction time, higher Oxford Sleep Resistance test omission error count adjusted for test duration (Oxford Sleep Resistance test_OMIS/MIN), and lower Oxford Sleep Resistance test and Maintenance of Wakefulness Test sleep latency compared with controls (all P < 0.01). Treatment with sodium oxybate was associated with a longer Maintenance of Wakefulness Test sleep latency (P < 0.01), lower Oxford Sleep Resistance test_OMIS/MIN (P = 0.01) and a lower Sustained Attention to Response Task error count (P = 0.01) in patients with narcolepsy, but not with absolute changes in Oxford Sleep Resistance test sleep latency or Psychomotor Vigilance Test reciprocal reaction time. It was concluded that portable measurements of sustained attention as well as in‐laboratory Oxford Sleep Resistance test and Maintenance of Wakefulness Test measurements revealed worse performance for narcoleptic patients compared with controls, and that sodium oxybate was associated with an improvement of sustained attention and a better resistance to sleep.     

Sleep extension versus nap or coffee,within the context of ‘sleep debt’

Though extended night‐time sleep mostly reduces the ‘afternoon dip’, little is known about evening benefits to alertness, or about comparisons with an afternoon nap or caffeine. Twenty healthy carefully screened adults, normal waking alertness levels, underwent four counterbalanced conditions: usual night sleep; night sleep extended<90 min (usual bed‐time); up to 20 min afternoon nap; and 150 mg afternoon caffeine (versus decaffeinated coffee). Sleepiness was measured by afternoon and evening multiple sleep latency test (MSLTs), longer psychomotor vigilance test (PVT) sessions and a subjective sleepiness scale. Sleep was extended by average of 74 min, and all participants could nap 15–20 min. Sleep extension had little effect on PVT determined modest levels of morning sleepiness. Afternoon and evening MSLTs showed all active treatments significantly reduced the ‘dip’, with nap most effective until mid‐evening; next effective was caffeine, then extension. Late evening sleepiness and subsequent sleep did not differ between conditions. Arguably, participants may have experienced some ‘sleep debt’, given they extended sleep and reflected some sleepiness within settings sensitive to sleepiness. Nevertheless, extended sleep seemed largely superfluous and inefficient in reducing modest levels of sleepiness when compared with a timely nap, and even caffeine. Sleep, such as food and fluid intakes, can be taken to excess of real biological needs, and for many healthy adults, there is a level of modest daytime sleepiness, only unmasked by very sensitive laboratory measures. It may reflect a requirement for more sleep or simply be within the bounds of normal acceptability.     

Self‐awakening improves alertness in the morning and during the day after partial sleep deprivation

The ability to awaken at a predetermined time without an alarm is known as self‐awakening. Self‐awakening improves morning alertness by eliminating sleep inertia; however, the effects of self‐awakening on daytime alertness and alertness that has deteriorated as a result of sleep loss are unknown. The aim of this study was to determine the effects of self‐awakening on both morning and daytime alertness after partial sleep deprivation. Fifteen healthy males without the habit of self‐awakening participated in a cross‐over trial including forced awakening and self‐awakening conditions. In each condition, participants' sleep was restricted to 5 h per night in their homes for 4 consecutive days. They completed a psychomotor vigilance task and subjective ratings of sleepiness immediately upon awakening each morning. On the fourth day, participants completed subjective ratings of sleepiness, a psychomotor vigilance task and sleep latency tests in the laboratory seven times at 1‐h intervals during the day. The response speed on the psychomotor vigilance task, in the morning and during the day, was higher in the self‐awakening than the forced awakening condition. Our results showed that self‐awakening improved alertness (assessed by response speeds) by reducing sleep inertia and alleviated daytime sleepiness heightened by partial sleep deprivation.     

Performance and alertness effects of caffeine, dextroamphetamine, and modafinil during sleep deprivation

Stimulants may provide short-term performance and alertness enhancement during sleep loss. Caffeine 600 mg, d-amphetamine 20 mg, and modafinil 400 mg were compared during 85 h of total sleep deprivation to determine the extent to which the three agents restored performance on simple psychomotor tasks, objective alertness and tasks of executive functions. Forty-eight healthy young adults remained awake for 85 h. Performance and alertness tests were administered bi-hourly from 8:00 hours day 2 to 19:00 hours day 5. At 23:50 hours on day 4 (after 64 h awake), subjects ingested placebo, caffeine 600 mg, dextroamphetamine 20 mg, or modafinil 400 mg (n=12 per group). Performance and alertness testing continued, and probe tasks of executive function were administered intermittently until the recovery sleep period (20:00 hours day 5 to 8:00 hours day 5). Bi-hourly postrecovery sleep testing occurred from 10:00 hours to 16:00 hours day 6. All three agents improved psychomotor vigilance speed and objectively measured alertness relative to placebo. Drugs did not affect recovery sleep, and postrecovery sleep performance for all drug groups was at presleep deprivation levels. Effects on executive function tasks were mixed, with improvement on some tasks with caffeine and modafinil, and apparent decrements with dextroamphetamine on others. At the doses tested, caffeine, dextroamphetamine, and modafinil are equally effective for approximately 2-4 h in restoring simple psychomotor performance and objective alertness. The duration of these benefits vary in accordance with the different elimination rates of the drugs. Whether caffeine, dextroamphetamine, and modafinil differentially restore executive functions during sleep deprivation remains unclear.     

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

Total sleep deprivation (TSD) is increasingly common in modern society bringing various neurobehavioural effects. Dynamic changes of behaviour performances during TSD have been reported extensively, while the cerebral activation underlying such changes have not been elucidated clearly. This study aimed to investigate dynamic changes in cerebral responses to the fastest and slowest psychomotor vigilance task (PVT) trials during TSD. Thirty‐six healthy subjects with intermediate chronotype performed the PVT while undergoing functional magnetic resonance imaging every 2 h from 22:00 hours on the first day to 06:00 hours on the second day (i.e. 22:00, 12:00, 02:00, 04:00 and 06:00 hours; a total of five imaging sessions). Behaviourally, significant time effects were found for the PVT performance. For imaging results, significant activation alterations were found in the cognitive control network and the default mode network (DMN) for the fastest and slowest PVT trials, respectively. Time–course analysis indicated that the largest differences for behavioural results and imaging results happened in session 4 and became more prominent in session 5. Our findings provide more detailed information about the process of sustained attention activation during one night of TSD and add information regarding the effect of circadian rhythmicity and homeostatic sleep pressure on regional brain responses.     

Exenatide improves excessive daytime sleepiness and wakefulness in obese patients with type 2 diabetes without obstructive sleep apnoea

We investigate the effects of exenatide on excessive daytime sleepiness (EDS), driving performance and depression score in patients with type 2 diabetes with EDS. Eight obese patients with diabetes but without obstructive sleep apnoea (OSA) participated in a placebo‐controlled single‐blind study during which multiple wakefulness and sleep latency test, Epworth score, driving performance, depression score, fasting glucose and glycated haemoglobin (HbA1c) levels were assessed at baseline, end of placebo and treatment phase at baseline and after 22 weeks of treatment. Mean (±standard error of the mean) age, body mass index (kg m²) and HbA1c [mmol mol^?1 (%)] of patients at baseline were 50 ± 4.9 years, 37.6 ± 1.1 and 65 ± 19 (8.06 ± 0.41), respectively. When compared to placebo, exenatide treatment was associated with a decrease in both subjective and objective sleepiness, based on the Epworth score reduction and the sleep latency increase assessed by multiple objective sleepiness and sustained attention (OSLER) tests, respectively. Mean sleep latency time (adjusted for change in HbA1c and weight) were 32.1 ± 1.7, 29.1 ± 1.7 and 37.7 ± 1.7, respectively (P = 0.002). Modelling for covariates suggested that improvement in mean sleep latency time is predicted by changes in weight (P = 0.003), but not by changes in HbA1c (P = 0.054). Epworth sleepiness score was reduced significantly (values for placebo versus exenatide: 11.3 ± 1.2 versus 5.7 ± 1.3; P = 0.003). No significant change was noted in the depression score and driving performance. Exenatide is associated with a significant reduction in objective sleepiness in obese patients with type 2 diabetes without OSA, independent of HbA1c levels. These findings could form a basis for further studies to investigate the pathophysiological mechanisms of sleepiness in obese patients with type 2 diabetes.     

Sleep enhances inhibitory behavioral control in discrimination learning in rats

Sleep supports the consolidation of memory, and it has been proposed that this enhancing effect of sleep pertains in particular to memories which are encoded under control of prefrontal–hippocampal circuitry into an episodic memory system. Furthermore, repeated reactivation and transformation of such memories during sleep are thought to promote the de-contextualization of these memories. Here, we aimed to establish a behavioral model for the study of such sleep-dependent system consolidation in rats, using a go/nogo conditional discrimination learning task known to essentially depend on prefrontal–hippocampal function. Different groups of rats were trained to criterion on this task and, then, subjected to 80-min retention intervals filled with spontaneous morning sleep, sleep deprivation, or spontaneous evening wakefulness. In a subsequent test phase, the speed of relearning of the discrimination task was examined as indicator of memory, whereby rats were either tested in the same context as during training or in a different context. Sleep promoted relearning of the conditional discrimination task, and this effect was similar for testing memory in the same or different context (p < 0.001). Independent of sleep and wakefulness during the retention interval, animals showed faster relearning when tested in the same context as during learning, compared with testing in a different context (p < 0.001). The benefitting effect of sleep on discrimination learning was primarily due to an enhancing effect on response suppression during the nogo stimulus. We infer from these results that sleep enhances memory for inhibitory behavioral control in a generalized context-independent manner and thereby might eventually also contribute to the abstraction of schema-like representations.     

Age-Related Reduction in Daytime Sleep Propensity and Nocturnal Slow Wave Sleep

Objective:

To investigate whether age-related and experimental reductions in SWS and sleep continuity are associated with increased daytime sleep propensity.

Methods:

Assessment of daytime sleep propensity under baseline conditions and following experimental disruption of SWS. Healthy young (20-30 y, n = 44), middle-aged (40-55 y, n = 35) and older (66-83 y, n = 31) men and women, completed a 2-way parallel group study. After an 8-h baseline sleep episode, subjects were randomized to 2 nights with selective SWS disruption by acoustic stimuli, or without disruption, followed by 1 recovery night. Objective and subjective sleep propensity were assessed using the Multiple Sleep Latency Test (MSLT) and the Karolinska Sleepiness Scale (KSS).

Findings:

During baseline sleep, SWS decreased (P < 0.001) and the number of awakenings increased (P < 0.001) across the 3 age groups. During the baseline day, MSLT values increased across the three age groups (P < 0.0001) with mean values of 8.7min (SD: 4.5), 11.7 (5.1) and 14.2 (4.1) in the young, middle-aged, and older adults, respectively. KSS values were 3.7 (1.0), 3.2 (0.9), and 3.4 (0.6) (age-group: P = 0.031). Two nights of SWS disruption led to a reduction in MSLT and increase in KSS in all 3 age groups (SWS disruption vs. control: P < 0.05 in all cases).

Conclusions:

Healthy aging is associated with a reduction in daytime sleep propensity, sleep continuity, and SWS. In contrast, experimental disruption of SWS leads to an increase in daytime sleep propensity. The age-related decline in SWS and reduction in daytime sleep propensity may reflect a lessening in homeostatic sleep requirement. Healthy older adults without sleep disorders can expect to be less sleepy during the daytime than young adults.

Citation:

Dijk DJ; Groeger JA; Stanley N; Deacon S. Age-related reduction in daytime sleep propensity and nocturnal slow wave sleep. SLEEP 2010;33(2):211-223.