Circadian and wake-dependent influences on subjective sleepiness, cognitive throughput, and reaction time performance in older and young adults

ACROSS A TYPICAL WAKING DAY, PERFORMANCE AND ALERTNESS ARE QUITE STABLE IN WELL-RESTED ADULTS.1 NEUROBEHAVIORAL PERFORMANCE has been shown to be influenced by both sleep-wake homeostatic (duration of prior wakefulness) and circadian (phase of the endogenous biological clock) influences. Achievement of stable performance and alertness across a normal ∼16-h waking day is hypothesized to result from the wake-dependent decline in alertness and performance being counterbalanced by an increasing wake-promoting signal from the circadian timing system that peaks towards the latter part of the habitual wake episode.2 Previous studies using designs that disrupt, restrict, and/or deprive subjects of sleep have all reported that subjective sleepiness and performance, including cognitive throughput, sustained vigilance, visual search tasks, and memory tasks, worsen with longer durations of time awake.1,3–5 Data from constant routine protocols in which subjects remain awake but in constant environmental and behavioral conditions have also shown that as time awake increases, performance decreases. These findings have been reported across a range of wake durations,1 including extreme conditions of up to 88 h of sleep deprivation.6 However, even under conditions of extreme sleep deprivation, progressive impairments in performance are reduced during the biological day compared to the biological night,1,6 an indication of the influence of the circadian timing system. This influence is such that for most measures, performance is best during the biological daytime and worst in the late biological nighttime, at or just after the circadian phase of the core body temperature nadir.1,6 The limitation of sleep deprivation protocols is that there is a confound between duration of prior wakefulness and circadian phase, and hence the independent contributions of each of these sleep-wake regulatory factors on performance cannot be estimated. The forced desynchrony protocol is a paradigm through which wake-dependent and circadian influences on performance in humans can be separated and quantified, and their interaction can be assessed. This protocol involves scheduling the subject to a rest-activity cycle duration much shorter or much longer than 24 h, beyond the range of entrainment of the circadian pacemaker.7 Using the forced desynchrony paradigm, we have reported previously that, in young adults, subjective alertness and neurobehavioral performance are affected by the duration of sustained wakefulness (a wake-dependent homeostatic process) as well as by a circadian process, and that these two processes interact such that the circadian influence on alertness and performance is stronger with greater durations of prior wakefulness.1,4,8 Similar results were achieved using imposed day lengths shorter (20 h, with 13.3 h wake),4 longer (28 h, with 18.7 h wake),1 and significantly longer than normal (42.85 h with 28.57 h wake).8 How these wake-dependent and circadian influences on performance may change with age has not been studied systematically. There are suggestions from sleep fragmentation and sleep deprivation studies that there may be age-related changes in both of these systems. An assessment of the effect of sleep fragmentation on performance in young and older subjects, in which subjects were aroused periodically throughout the sleep episode, found the performance of older subjects to be less sensitive to sleep disturbance than younger subjects,9 suggesting an age-related attenuation of the wake-dependent homeostatic influence on performance. Assessment of the response of young and older subjects to varying durations of sleep deprivation has also been performed. In a study conducted in our laboratory, we found that older adults were better able than young adults to maintain alertness and sustained attention across 26 h.10 Similar results were obtained from a study of 40 h of sleep deprivation in young and older subjects, in which the authors reported that older subjects were able to maintain virtually stable reaction time performance while younger subjects showed greater performance impairments.11 In addition to sleep fragmentation and sleep deprivation studies, results from sleep restriction studies have also suggested that older adults are less susceptible to circadian and wake-dependent performance decrements.12,13 While there is evidence from those prior studies that there may be modifications in both the circadian and wake-dependent homeostatic influences on performance with aging, the designs used in those studies did not allow for the separation of circadian and homeostatic influences, and therefore in most cases, circadian and wake-dependent influences were confounded. Therefore, one purpose of our present analysis was to separate the wake-dependent and circadian influences on performance in older adults to quantify their relative influences, and to compare those findings with results from young adults. In addition, most prior reports on performance in young adults from forced desynchrony studies averaged data across the entire forced desynchrony segment (typically 3-4 weeks), leaving open the possibility that the circadian and/or wake-dependent influence on performance might change across such a long experiment. A second purpose of the present analysis was therefore to examine subjective alertness and performance with respect to how long subjects were exposed to the repeated circadian phase misalignment inherent in forced desynchrony, and to determine whether this differed between young and older subjects. We selected subjective alertness and performance data from older subjects who participated in a 20-h forced desynchrony study and compared them with data previously-reported from young subjects in a 20-h forced desynchrony study.4