David Darwent

Sleep, Wake and Phase Dependent Changes in Neurobehavioral Function under Forced Desynchrony

STUDY OBJECTIVES The homeostatic-circadian regulation of neurobehavioral functioning is not well understood in that the role of sleep dose in relation to prior wake and circadian phase remains largely unexplored. The aim of the present study was to examine the neurobehavioral impact of sleep dose at different combinations of prior wake and circadian phase. DESIGN A between-participant design involving 2 forced desynchrony protocols varying in sleep dose. Both protocols comprised 7 repetitions of a 28-h sleep/wake cycle. The sleep dose in a standard protocol was 9.33 h per 28-h day and 4.67 h in a sleep-restricted protocol. SETTING A time-isolation laboratory at the Centre for Sleep Research, the University of South Australia. PARTICIPANTS A total of 27 young healthy males participated in the study with 13 in the standard protocol (age 22.5 ± 2.2 y) and 14 in the sleep-restricted protocol (age 21.8 ± 3.8 y). INTERVENTIONS Wake periods during both protocols were approximately 4 h delayed each 28-h day relative to the circadian system, allowing performance testing at different combinations of prior wake and circadian phase. The manipulation in sleep dose between the 2 protocols, therefore, allowed the impact of sleep dose on neurobehavioral performance to be examined at various combinations of prior wake and circadian phase. MEASUREMENTS AND RESULTS Neurobehavioral function was assessed using the psychomotor vigilance task (PVT). There was a sleep dose × circadian phase interaction effect on PVT performance such that sleep restriction resulted in slower and more variable response times, predominantly during the biological night. This interaction was not altered by prior wakefulness, as indicated by a nonsignificant sleep dose × circadian phase × prior wake interaction. CONCLUSIONS The performance consequence of sleep restriction in our study was prominent during the biological night, even when the prior wake duration was short, and this performance consequence was in forms of waking state instability. This result is likely due to acute homeostatic sleep pressure remaining high despite the sleep episode.

Mismatch between subjective alertness and objective performance under sleep restriction is greatest during the biological night

Subjective alertness may provide some insight into reduced performance capacity under conditions suboptimal to neurobehavioural functioning, yet the accuracy of this insight remains unclear. We therefore investigated whether subjective alertness reflects the full extent of neurobehavioural impairment during the biological night when sleep is restricted. Twenty‐seven young healthy males were assigned to a standard forced desynchrony (FD) protocol (n = 13; 9.33 h in bed/28 h day) or a sleep‐restricted FD protocol (n = 14; 4.67 h in bed/28 h day). For both protocols, subjective alertness and neurobehavioural performance were measured using a visual analogue scale (VAS) and the psychomotor vigilance task (PVT), respectively; both measures were given at various combinations of prior wake and circadian phase (biological night versus biological day). Scores on both measures were standardized within individuals against their respective baseline average and standard deviation. We found that PVT performance and VAS rating deviated from their respective baseline to a similar extent during the standard protocol, yet a greater deviation was observed for PVT performance than VAS rating during the sleep‐restricted protocol. The discrepancy between the two measures during the sleep‐restricted protocol was particularly prominent during the biological night compared with the biological day. Thus, subjective alertness did not reflect the full extent of performance impairment when sleep was restricted, particularly during the biological night. Given that subjective alertness is often the only available information upon which performance capacity is assessed, our results suggest that sleep‐restricted individuals are likely to under‐estimate neurobehavioural impairment, particularly during the biological night.

The sleep and performance of train drivers during an extended freight-haul operation

The sleep and performance of train drivers was monitored across a 106-h rail operation between the Australian cities of Adelaide and Perth. The drivers worked alternating 8-h shift rotations across the operation and rested in specially equipped, crew-van carriages during non-work periods. The crew-van rest opportunities were associated with shorter bedtime spans, less total sleep time, and poorer sleep efficiency than sleeps initiated at home. The duration of crew-van sleeps was primarily dependent on the time of day at which the rest opportunities occurred. Overall, drivers incurred a significant cumulative sleep loss across the duration of the operation. Despite the deficit, drivers were able to sustain vigilance performance across the operation.

CONTRIBUTION OF CORE BODY TEMPERATURE, PRIOR WAKE TIME, AND SLEEP STAGES TO COGNITIVE THROUGHPUT PERFORMANCE DURING FORCED DESYNCHRONY

Shiftworkers are often required to sleep at inappropriate phases of their circadian timekeeping system, with implications for the dynamics of ultradian sleep stages. The independent effects of these changes on cognitive throughput performance are not well understood. This is because the effects of sleep on performance are usually confounded with circadian factors that cannot be controlled under normal day/night conditions. The aim of this study was to assess the contribution of prior wake, core body temperature, and sleep stages to cognitive throughput performance under conditions of forced desynchrony (FD). A total of 11 healthy young adult males resided in a sleep laboratory in which day/night zeitgebers were eliminated and ambient room temperature, lighting levels, and behavior were controlled. The protocol included 2 training days, a baseline day, and 7 × 28-h FD periods. Each FD period consisted of an 18.7-h wake period followed by a 9.3-h rest period. Sleep was assessed using standard polysomnography. Core body temperature and physical activity were assessed continuously in 1-min epochs. Cognitive throughput was measured by a 5-min serial addition and subtraction (SAS) task and a 90-s digit symbol substitution (DSS) task. These were administered in test sessions scheduled every 2.5 h across the wake periods of each FD period. On average, sleep periods had a mean (± standard deviation) duration of 8.5 (±1.2) h in which participants obtained 7.6 (±1.4) h of total sleep time. This included 4.2 (±1.2) h of stage 1 and stage 2 sleep (S1–S2 sleep), 1.6 (±0.6) h of slow-wave sleep (SWS), and 1.8 (±0.6) h of rapid eye movement (REM) sleep. A mixed-model analysis with five covariates indicated significant fixed effects on cognitive throughput for circadian phase, prior wake time, and amount of REM sleep. Significant effects for S1–S2 sleep and SWS were not found. The results demonstrate that variations in core body temperature, time awake, and amount of REM sleep are associated with changes in cognitive throughput performance. The absence of significant effect for SWS may be attributable to the truncated range of sleep period durations sampled in this study. However, because the mean and variance for SWS were similar to REM sleep, these results suggest that cognitive throughput may be more sensitive to variations in REM sleep than SWS. (Author correspondence: david.darwent@unisa.edu.au)

The effect of sleep restriction on snacking behaviour during a week of simulated shiftwork

Due to irregular working hours shiftworkers experience circadian disruption and sleep restriction. There is some evidence to indicate that these factors adversely affect health through changes in snacking behaviour. The aim of this study was to investigate the impact of sleep restriction, prior wake and circadian phase on snacking behaviour during a week of simulated shiftwork. Twenty-four healthy males (age: 22.0 ± 3.6 years, mean ± SD) lived in a sleep laboratory for 12 consecutive days. Participants were assigned to one of two schedules: a moderate sleep restriction condition (n=10) equivalent to a 6-h sleep opportunity per 24h or a severe sleep restriction condition (n=14) equivalent to a 4-h sleep opportunity per 24h. In both conditions, sleep/wake episodes occurred 4h later each day to simulate a rotating shiftwork pattern. While living in the laboratory, participants were served three meals and were provided with either five (moderate sleep restriction condition) or six (severe sleep restriction condition) snack opportunities daily. Snack choice was recorded at each opportunity and assigned to a category (sweet, savoury or healthy) based on the content of the snack. Data were analysed using a Generalised Estimating Equations approach. Analyses show a significant effect of sleep restriction condition on overall and sweet snack consumption. The odds of consuming a snack were significantly greater in the severe sleep restriction condition (P<0.05) compared to the moderate sleep restriction condition. In particular, the odds of choosing a sweet snack were significantly increased in the severe sleep restriction condition (P<0.05). Shiftworkers who are severely sleep restricted may be at risk of obesity and related health disorders due to elevated snack consumption and unhealthy snack choice. To further understand the impact of sleep restriction on snacking behaviour, future studies should examine physiological, psychological and environmental motivators.

The influence of circadian phase and prior wake on neuromuscular function.

Previous forced desynchrony (FD) studies have shown that neurobehavioral function is affected by circadian phase and duration of prior wakefulness. There is some evidence that neuromuscular function may also be affected by circadian phase and prior wake, but these effects have not been systematically investigated. This study examined the effects of circadian phase and prior wake on two measures of neuromuscular function—postural balance (PB) and maximal grip strength (MGS)—using a 28-h FD protocol. Eleven male participants (mean ± SD: 22.7 ± 2.5 yr) lived in a sound-attenuated, light- and temperature-controlled time-isolation laboratory for 12 days. Following two training days and a baseline day, participants were scheduled to seven 28-h FD days, with the ratio between sleep opportunity and wake spans kept constant (i.e., 9.3 h sleep period and 18.7 h wake period). PB was measured during 1 min of quiet standing on a force platform. MGS of the dominant hand was measured using a dynamometer. These two measures were obtained every 2.5 h during wake. Core body temperature was continuously recorded with rectal thermistors to determine circadian phase. For both measures of neuromuscular function, individual data points were assigned a circadian phase and a level of prior wake. Data were analyzed by repeated-measures analysis of variance (ANOVA) with two within-subjects factors: circadian phase (six phases) and prior wake (seven levels). For MGS, there was a main effect of circadian phase, but no main effect of prior wake. For PB, there were no main effects of circadian phase or prior wake. There were no interactions between circadian phase and prior wake for MGS or PB. The significant effect of circadian phase on muscle strength is in agreement with previous reports in the literature. In terms of prior wake, both MGS and PB remained relatively stable across wake periods, indicating that neuromuscular function may be more robust than neurobehavioral function when the duration of wakefulness is within a normal range (i.e., 18.7 h). (Author correspondence: charli.sargent@unisa.edu.au)

Long-haul pilots use in-flight napping as a countermeasure to fatigue

The aim of this study was to examine the effects of fatigue on the amount of in-flight sleep obtained by airline pilots during long-haul duty periods. A total of 301 pilots collected sleep/wake and work/rest data for a period of at least 2 weeks each. Fatigue likelihood, i.e. low, moderate, high, or extreme, was estimated for each duty period based on a pilots sleep/wake behaviour prior to duty and the time of day that the duty period occurred. Participants obtained 1.8 h of sleep (i.e. 27% of their rest time) during duty periods with low fatigue likelihood and 3.7 h of sleep (i.e. 54% of their rest time) during duty periods with extreme fatigue likelihood. These results indicate that (i) long-haul pilots obtain substantially more sleep during duty periods when fatigue is likely to be extreme than when fatigue is likely to be low and (ii) long-haul pilots use in-flight napping as a fatigue countermeasure, but more could be done to increase its efficacy.

The influence of circadian time and sleep dose on subjective fatigue ratings.

Subjective ratings of fatigue are increasingly being used as part of a suite of tools to assess fatigue-related risk on the road and in the workplace. There is some debate however, as to whether individuals can accurately gauge their own fatigue states, particularly under conditions of sleep restriction. It is also unclear which references are used by individuals to assess fatigue - for example prior sleep, time of day, workload, or previous ratings. The current study used a sophisticated laboratory protocol to examine the independent contributions of sleep, circadian phase and sleep debt to fatigue ratings. Importantly, participants had no knowledge of time of day, how much sleep they were getting, or how long they were awake. Twenty-eight healthy, young males participated in one of two conditions of a 28 h forced desynchrony protocol - severe sleep restriction (4.7h sleep and 23.3h wake) or moderate sleep restriction (7h sleep and 21 h wake). Fatigue ratings were provided prior to and following each sleep period using the Samn-Perelli fatigue scale. Repeated measures ANOVAs were used to analyse the effects of circadian phase, sleep dose and study day. Results demonstrated an effect of circadian phase on both pre-sleep and post-sleep fatigue ratings. The significant effect of study day is interpreted as an effect of circadian time, as opposed to accumulating sleep debt. An effect of sleep dose was only seen in post-sleep fatigue ratings. The findings suggest that post-sleep fatigue ratings may be sensitive to prior sleep and may be useful as an indicator of fatigue-related risk, particularly when triangulated with information about recent total sleep time.

Sleep Restriction Masks the Influence of the Circadian Process on Sleep Propensity

Previous forced desynchrony studies have highlighted the close relationship between the circadian rhythms of core body temperature (CBT) and sleep propensity. In particular, these studies have shown that a “forbidden zone” for sleep exists on the rising limb of the CBT rhythm. In these previous studies, the length of the experimental day was either ultrashort (90 min), short (20 h), or long (28 h), and the ratio of sleep to wake was normal (i.e., 1:2). The aim of the current study was to examine the relative effects of the circadian and homeostatic processes on sleep propensity using a 28-h forced desynchrony protocol in which the ratio of sleep to wake was substantially lower than normal (i.e., 1:5). Twenty-seven healthy males lived in a time-isolation sleep laboratory for 11 consecutive days. Participants completed either a control (n = 13) or sleep restriction (n = 14) condition. In both conditions, the protocol consisted of 2 × 24-h baseline days followed by 8 × 28-h forced desynchrony days. On forced desynchrony days, the control group had 9.3 h in bed and 18.7 h of wake, and the sleep restriction group had 4.7 h in bed and 23.3 h of wake. For all participants, each 30-s epoch of time in bed was scored as sleep or wake based on standard polysomnography recordings, and was also assigned a circadian phase (360° = 24 h) based on a cosine equation fitted to continuously recorded CBT data. For each circadian phase (i.e., 72 × 5° bins), sleep propensity was calculated as the percentage of epochs spent in bed scored as sleep. For the control group, there was a clear circadian rhythm in sleep propensity, with a peak of 98.5% at 5° (∼05:20 h), a trough of 64.9% at 245° (∼21:20 h), and an average of 82.3%. In contrast, sleep propensity for the sleep restriction group was relatively high at all circadian phases, with an average of 96.7%. For this group, the highest sleep propensity (99.0%) occurred at 60° (∼09:00 h), and the lowest sleep propensity (91.3%) occurred at 265° (∼22:40 h). As has been shown previously, these current data indicate that with a normal sleep-to-wake ratio, the effect of the circadian process on sleep propensity is pronounced, such that a forbidden zone for sleep exists at a phase equivalent to evening time for a normally entrained individual. However, these current data also indicate that when the ratio of sleep to wake is substantially lower than normal, this circadian effect is masked. In particular, sleep propensity is very high at all circadian phases, including those that coincide with the forbidden zone for sleep. This finding suggests that if the homeostatic pressure for sleep is sufficiently high, then the circadian drive for wakefulness can be overridden. In future studies, it will be important to determine whether or not this masking effect occurs with less severe sleep restriction, e.g., with a sleep-to-wake ratio of 1:3. (Author correspondence: charli.sargent@cqu.edu.au)

The Validity of Temperature-Sensitive Ingestible Capsules for Measuring Core Body Temperature in Laboratory Protocols

The human core body temperature (CBT) rhythm is tightly coupled to an endogenous circadian pacemaker located in the suprachiasmatic nucleus of the anterior hypothalamus. The standard method for assessing the status of this pacemaker is by continuous sampling of CBT using rectal thermometry. This research sought to validate the use of ingestible, temperature-sensitive capsules to measure CBT as an alternative to rectal thermometry. Participants were 11 young adult males who had volunteered to complete a laboratory protocol that extended across 12 consecutive days. A total of 87 functional capsules were ingested and eliminated by participants during the laboratory internment. Core body temperature samples were collected in 1-min epochs and compared to paired samples collected concurrently via rectal thermistors. Agreement between samples that were collected using ingestible sensors and rectal thermistors was assessed using the gold-standard limits of agreement method. Across all valid paired samples collected during the study (n = 120,126), the mean difference was 0.06°C, whereas the 95% CI (confidence interval) for differences was less than ±0.35°C. Despite the overall acceptable limits of agreement, systematic measurement bias was noted across the initial 5 h of sensor-transit periods and attributed to temperature gradations across the alimentary canal. (Author correspondence: david.darwent@unisa.edu.au)