Sleep Deprivation and Caffeine Treatment Potentiate Photic Resetting of the Master Circadian Clock in a Diurnal Rodent

Jha, Pawan Kumar; Bouâouda, Hanan; Gourmelen, Sylviane; Dumont, Stéphanie; Fuchs, F.; Goumon, Yannick; Bourgin, Patrice; Kalsbeek, Andries; Challet, Étienne

doi:10.1523/jneurosci.3241-16.2017

Cited by 33 publications

(39 citation statements)

References 49 publications

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“…In contrast, repeated caffeine intake in the morning did not successfully entrain three blind patients [42]. Furthermore, a recent animal study under constant conditions suggests that caffeine treatment does only potentiate light-induced phase shifts when given at the end of the active phase or during rest, but not at start of the active phase [43]. Together with the present results, the evidence suggests that the circadian system seems to be particularly sensitive to caffeine when given at the end of the biological day.…”

Section: Discussionmentioning

confidence: 89%

Caffeine-dependent changes of sleep-wake regulation: evidence for adaptation after repeated intake

Weibel

Lin

Landolt

et al. 2019

Preprint

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To enhance wakefulness, daily consumption of caffeine in the morning and afternoon is highly common. However, it is unknown whether such a regular intake pattern affects timing and quality of wakefulness, as regulated by an interplay of circadian and sleep-homeostatic mechanisms. Thus, we investigated the effects of daily caffeine intake and its withdrawal on circadian rhythms and wake-promotion in 20 male young habitual caffeine consumers. We applied a double-blind, within-subject design with a caffeine (150 mg, 3 x daily), a placebo, and a withdrawal condition each lasting ten days. Starting on day nine of treatment, salivary melatonin and cortisol, evening nap sleep, as well as sleepiness and vigilance performance throughout day and night were quantified during 43 h under controlled laboratory conditions.Neither the time course of melatonin (i.e., onset, amplitude, or area under the curve) nor the time course of cortisol were significantly affected by caffeine intake or its withdrawal. During withdrawal, however, volunteers reported increased sleepiness, showed more attentional lapses, as well as polysomnography-derived markers of elevated sleep propensity in the late evening compared to both, placebo and caffeine conditions. Thus, the typical timing of habitual caffeine intake in humans may not necessarily shift circadian phase nor lead to clear-cut benefits in alertness. The time-of-day independent effects of caffeine withdrawal suggest an adaptation to the substance, presumably in the homeostatic aspect of sleepwake regulation.Caffeine, caffeine withdrawal, and sleep-wake regulation

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Section: Discussionmentioning

confidence: 89%

Caffeine-dependent changes of sleep-wake regulation: evidence for adaptation after repeated intake

Weibel

Lin

Landolt

et al. 2019

Preprint

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“…More recently it was found in the grass rat ( Arvicanthis ansorgei ), a day active rodent, that sleep deprivation enhances light induced phase shifts (Jha et al, 2017). In contrast to previous findings, it was suggested that diurnal animals will show increased phase shifting after sleep deprivation, whereas nocturnal animals will show a decrease.…”

Section: The Influence Of the Homeostatmentioning

confidence: 99%

Sleep homeostasis and the circadian clock: Do the circadian pacemaker and the sleep homeostat influence each other’s functioning?

Deboer

2018

Neurobiology of Sleep and Circadian Rhythms

154

113

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Sleep is regulated by a homeostatic and a circadian process. Together these two processes determine most aspects of sleep and related variables like sleepiness and alertness. The two processes are known to be able to work independently, but also to both influence sleep and sleep related variables in an additive or more complex manner. The question remains whether the two processes are directly influencing each other. The present review summarizes evidence from behavioural and electroencephalographic determined sleep, electrophysiology, gene knock out mouse models, and mathematical modelling to explore whether sleep homeostasis can influence circadian clock functioning and vice versa . There is a multitude of data available showing parallel action or influence of sleep homeostatic mechanisms and the circadian clock on several objective and subjective variables related to sleep and alertness. However, the evidence of a direct influence of the circadian clock on sleep homeostatic mechanisms is sparse and more research is needed, particularly applying longer sleep deprivations that include a second night. The strongest evidence of an influence of sleep homeostatic mechanisms on clock functioning comes from sleep deprivation experiments, demonstrating an attenuation of phase shifts of the circadian rhythm to light pulses when sleep homeostatic pressure is increased. The data suggest that the circadian clock is less susceptible to light when sleep pressure is high. The available data indicate that a strong central clock will induce periods of deep sleep, which in turn will strengthen clock function. Both are therefore important for health and wellbeing. Weakening of one will also hamper functioning of the other. Shift work and jet lag are situations where one tries to adapt to zeitgebers in a condition where sleep is compromised. Adaptation to zeitgebers may be improved by introducing nap schedules to reduce sleep pressure, and through that increasing clock susceptibility to light.

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“…Moreover, it remains to be elucidated which component within the human circadian timing system is affected by caffeine and majorly regulates caffeine-induced shifts in melatonin secretion. A blockade of adenosine receptors might change light responses at the level of the retina (99) or the central circadian master-clock (50,100) or may even affect melatonin release at the pineal gland (101).…”

Section: Discussionmentioning

confidence: 99%

“…The dose of 80 mg roughly equals not only the daily average intake of adolescents in the US (3, 5) but also the content per serving in a range of common energy drinks (e.g., Bomb Energy Drink® ( ). We set the timing of administration to the evening hours to allow maximal effects of caffeine on both sleep (39,48,49) and circadian rhythms (31,50). Please note that teenagers represent the age group in which evening caffeine consumption is most common (5).…”

Section: Study Protocolmentioning

confidence: 99%

Wide awake at bedtime? The effects of caffeine on sleep and circadian timing in teenagers - a randomized crossover trial

Reichert

Veitz

Bühler

et al. 2020

Preprint

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Background: Adolescents frequently consume caffeine with unknown consequences on sleep and circadian rhythms. In adults, the evidence indicates that caffeine acutely reduces homeostatic sleep pressure and delays the circadian timing system.Objective: Here, we investigated the acute effects of caffeine intake on the developing sleep-wake regulatory system of teenagers.Design: In a double-blind randomized crossover laboratory study, 18 teenagers (16.1 ± 1 years old, pubertal development scale [PDS]: 2.76 ± 0.35) ingested 80 mg caffeine (vs placebo) four hours prior to bedtime. Until bedtime, participants regularly filled in the Karolinska Sleepiness Scale and gave saliva samples to measure melatonin secretion. During nighttime, we quantified homeostatic sleep need by the electroencephalographically derived amount of slow wave sleep duration (SWS). After sleep, participants rated sleep quality by the Leeds Sleep Evaluation Questionnaire.Results: While participants felt less sleepy after caffeine vs. placebo (P=0.038), their ratings of sleep quality were not strongly affected by the treatment. However, objectively, SWS was on average reduced by ~20 min after caffeine vs. placebo (P=0.026). This caffeine-induced reduction was more pronounced in those individuals with more SWS under placebo (regression: P=0.042; standardized beta=0.622, P=0.011), even if controlling for habitual caffeine intake or pubertal stage (PDS). In melatonin onsets we observed both delays and advances in response to caffeine. This variance could partly be explained by differences in relative dose (i.e., mg caffeine/kg of bodyweight): the higher the relative dose, the more likely were delays (regression: P=0.01; standardized beta=0.592, P=0.01).Conclusions: In teenagers, evening caffeine intake of already 80 mg (i.e. ~8fl oz of common energy drinks) is sufficient to promote alertness at the costs of subsequent sleep. These costs might be more pronounced in adolescents with a higher need for SWS. Moreover, caffeine might disturb the circadian timing system, consequently hampering the balanced interplay of sleep-wake regulatory components.

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Sleep Deprivation and Caffeine Treatment Potentiate Photic Resetting of the Master Circadian Clock in a Diurnal Rodent

Cited by 33 publications

References 49 publications

Caffeine-dependent changes of sleep-wake regulation: evidence for adaptation after repeated intake

Caffeine-dependent changes of sleep-wake regulation: evidence for adaptation after repeated intake

Sleep homeostasis and the circadian clock: Do the circadian pacemaker and the sleep homeostat influence each other’s functioning?

Wide awake at bedtime? The effects of caffeine on sleep and circadian timing in teenagers - a randomized crossover trial

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