Sleep inertia, sleep homeostatic and circadian influences on higher‐order cognitive functions

Abstract

Summary Sleep inertia, sleep homeostatic, and circadian processes modulate cognition, including reaction time, memory, mood, and alertness. How these processes influence higher-order cognitive functions is not well known. Six participants completed a 73-daylong study that included two 14-daylong 28h forced desynchrony protocols, to examine separate and interacting influences of sleep inertia, sleep homeostasis, and circadian phase on higher-order cognitive functions of inhibitory control and selective visual attention. Cognitive performance for most measures was impaired immediately after scheduled awakening and improved over the first ~2-4h of wakefulness (sleep inertia); worsened thereafter until scheduled bedtime (sleep homeostasis); and was worst at ~60° and best at ~240° (circadian modulation, with worst and best phases corresponding to ~9AM and ~9PM respectively, in individuals with a habitual waketime of 7AM). The relative influences of sleep inertia, sleep homeostasis, and circadian phase depended on the specific higher-order cognitive function task examined. Inhibitory control appeared to be modulated most strongly by circadian phase, whereas selective visual attention for a spatial-configuration search task was modulated most strongly by sleep inertia. These findings demonstrate that some higher-order cognitive processes are differentially sensitive to different sleep-wake regulatory processes. Differential modulation of cognitive functions by different sleep-wake regulatory processes has important implications for understanding mechanisms contributing to performance impairments during adverse circadian phases, sleep deprivation, and/or upon awakening from sleep.

Sex differences in the circadian regulation of sleep and waking cognition in humans

“…This finding is in accordance with the results obtained in a similar forced desynchrony protocol (26) and in a quantitative analysis of the effects of 36 h of wakefulness across nearly 1.5 circadian cycles (51). In accordance with previous observations (27)(28)(29), both the linear and nonlinear analyses demonstrated that the effects of time awake and circadian phase interacted: The deterioration with time awake is most pronounced in the early morning; in other words, the effect of circadian phase on performance very much depends on time awake.…”

“…In the present study, the deterioration of brain function was observed even though time awake varied only between 0 and ∼19 h. This deterioration was modulated by circadian phase so that it was more pronounced when wakefulness coincided with the phase of melatonin secretion, i.e., the biological night. In one previous study with a number of tasks similar to that in our study, circadian effect sizes for sleepiness and attention were relatively pronounced, in accordance with the current study (26). However, inhibition was more affected by circadian phase in that study than in our study, where aspects of inhibition assessed in SART did not show comparably large circadian effects.…”

“…Under these conditions of forced desynchrony, various aspects of waking performance continue to display nearly a 24-h rhythmicity in synchrony with the melatonin rhythm in addition to the rhythmicity associated with the sleepwake cycle (26)(27)(28)(29). Some of the putative mechanisms by which circadian rhythmicity may contribute to brain function, e.g., the circadian modulation of synaptic plasticity independent of vigilance, have been identified (30).…”

Diurnal and circadian variation of sleep and alertness in men vs. naturally cycling women

“…Controlling for both circadian phase and homeostatic sleep pressure using a forced desynchrony protocol, Scheer et al (34) demonstrated that the effect of sleep inertia on performance was gone within 20 min across all circadian phases. Conversely, others, albeit using protocols that did not assess throughout all circadian phases (35) or with infrequent assessments postawakening (36), have reported that sleep inertia can take longer periods to dissipate (between 2 and 4 h). We also did not include an objective measure of performance, although our results are consistent with those of others who did (25).…”

Waking up is the hardest thing I do all day: Sleep inertia and sleep drunkenness

“…In a forced desynchrony protocol designed to tease apart these factors, Burke et al demonstrated that the largest effect sizes from sleep inertia were on selective visual attention (on a spatial search task) and subjective sleepiness [40]. Forced desynchrony studies have confirmed that impaired performance on awakening is most prominent during the biological night, when awakening at or within 120° before the core body temperature minimum [41, 42].…”