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Circadian and wakefulness-sleep modulation of cognition in humans - PubMed

  • ️Sun Jan 01 2012

Circadian and wakefulness-sleep modulation of cognition in humans

Kenneth P Wright et al. Front Mol Neurosci. 2012.

Abstract

Cognitive and affective processes vary over the course of the 24 h day. Time of day dependent changes in human cognition are modulated by an internal circadian timekeeping system with a near-24 h period. The human circadian timekeeping system interacts with sleep-wakefulness regulatory processes to modulate brain arousal, neurocognitive and affective function. Brain arousal is regulated by ascending brain stem, basal forebrain (BF) and hypothalamic arousal systems and inhibition or disruption of these systems reduces brain arousal, impairs cognition, and promotes sleep. The internal circadian timekeeping system modulates cognition and affective function by projections from the master circadian clock, located in the hypothalamic suprachiasmatic nuclei (SCN), to arousal and sleep systems and via clock gene oscillations in brain tissues. Understanding the basic principles of circadian and wakefulness-sleep physiology can help to recognize how the circadian system modulates human cognition and influences learning, memory and emotion. Developmental changes in sleep and circadian processes and circadian misalignment in circadian rhythm sleep disorders have important implications for learning, memory and emotion. Overall, when wakefulness occurs at appropriate internal biological times, circadian clockwork benefits human cognitive and emotion function throughout the lifespan. Yet, when wakefulness occurs at inappropriate biological times because of environmental pressures (e.g., early school start times, long work hours that include work at night, shift work, jet lag) or because of circadian rhythm sleep disorders, the resulting misalignment between circadian and wakefulness-sleep physiology leads to impaired cognitive performance, learning, emotion, and safety.

Keywords: circadian phase; circadian sleep disorders; forced desynchrony; performance; sleep homeostasis.

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Figures

Figure 1
Figure 1

(A) Brain arousal for neurocognitive and neuro-affective function is promoted by ascending brain stem, forebrain and hypothalamic projections to the cortex and midbrain. Neurotransmitter and neuropeptide systems involved in brain arousal and therefore in cognitive and affective function include the monoaminergic neurotransmitters histamine (His) from the tuberomammillary nucleus (TMN), norepinephrine (NE) from the locus coeruleus (LC), serotonin (5-HT) from the midbrain raphe nuclei, dopamine (DA) from the ventral tegmental area (VTA), and substantia nigra (not shown); the cholinergic neurotransmitter acetylcholine (ACh) from the basal forebrain (BF) and the pedunculopontine (PPT), and laterodorsal tegmental nuclei (LDT); the peptide orexin (ORX), also referred to as hypocretin, from the lateral hypothalamus (LH); the excitatory amino acids glutamate (GLUT) and aspartate; vasopressin (VP), and vasoactive intestinal polypeptide (VIP) from the suprachiasmatic nuclei (SCN). (B) The master circadian clock located in the SCN has modulatory input to many of the ascending arousal pathways, some through direct projections from the SCN (not labeled, see text) and many through indirect projections relayed by the dorsomedial hypothalamus (DMH). Through such projections, the SCN can modulate circadian rhythms in brain arousal to promote wakefulness. (C) The SCN has modulatory input to the sleep systems via relay projections to the DMH, onto the sleep promoting VLPO as well as midbrain and brain stem arousal systems. Through such projections, the SCN can modulate circadian rhythms in brain arousal to promote sleep.

Figure 2
Figure 2

Typical pattern of cognition across the day and one night of total sleep deprivation. Sleep inertia initially impairs cognition following the transition from sleep to wakefulness. Cognition improves rapidly within the first 20 min following awakening and continues to improve over the first ∼2–4 h of wakefulness. Cognition remains high for the first ∼8 h awake, often followed by a midafternoon dip in cognition and then improved cognition until immediately before habitual bedtime. Cognition is impaired by staying awake overnight. Horizontal line represents the average performance across the day. Reprinted with permission from (Wertz et al., 2006).

Figure 3
Figure 3

Simplified model of wakefulness-sleep and circadian modulation of cognition. Data are double plotted and show individual contribution of sleep inertia (grogginess upon awakening from sleep), homeostatic sleep drive (time awake and prior sleep history) and circadian phase (internal biological time) modulation of cognitive function under typical conditions.

Figure 4
Figure 4

Delayed Sleep Phase (DSP). Delayed sleep phase is the most common wakefulness-sleep challenge in adolescents and may lead to a DSP circadian sleep disorder. Individuals with DSP report difficulty falling asleep and difficulty awakening at the times required by school/work schedules. The phase delay in circadian timing, as indicated in this schematic by the later melatonin rhythm, may be related to biological (circadian physiology) and behavioral (e.g., social activities, increased light exposure in the evening, earlier school start times) changes that occur during adolescence. DSP combined with early school start times is thought to contribute to poor school performance and reduced sleep leading to chronic sleep loss during the week (open box).

Figure 5
Figure 5

Simplified model of wakefulness-sleep and circadian modulation of cognition during circadian misalignment associated with night work. Data are double plotted and show individual contributions of sleep inertia (grogginess upon awakening from sleep), homeostatic sleep drive (time awake and prior sleep history) and circadian phase (internal biological time) modulation of cognitive function. The interaction between sleep inertia, homeostatic sleep drive and circadian phase are altered during night shift work as compared to day work shown in Figure 3 such that sleepiness is promoted during the work shift.

Figure 6
Figure 6

Schematic of the integration of sleep inertia, sleep homeostatic and circadian control systems that modulate cognition, affect, physiology and behavior. Homeostatic sleep drive, circadian rhythms and sleep inertia all interact to influence human cognition, physiology and behavior. Arrows represent direction of influence. Circadian phase and homeostatic sleep drive interact to influence each other and both processes modulate sleep inertia. All three processes independently, and perhaps interactively, influence cognition, affect, physiology, and behavior. Behavior also feeds back to alter sleep homeostasis (e.g., choice to sleep versus engage in other activities) and circadian physiology (e.g., gating of exposure to light).

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