Christina Schmidt

A time to think: circadian rhythms in human cognition.

Although peaks and troughs in cognitive performance characterize our daily functioning, time-of-day fluctuations remain marginally considered in the domain of cognitive psychology and neuropsychology. Here, we attempt to summarize studies looking at the effects of sleep pressure, circadian variations, and chronotype on cognitive functioning in healthy subjects. The picture that emerges from this assessment is that beyond physiological variables, time-of-day modulations affect performance on a wide range of cognitive tasks measuring attentional capacities, executive functioning, and memory. These performance fluctuations are also contingent upon the chronotype, which reflects interindividual differences in circadian preference, and particularly upon the synchronicity between the individuals peak periods of circadian arousal and the time of the day at which testing occurs. In themselves, these conclusions should direct both the clinicians and the researchers attention towards the utmost importance to account for time-of-day parameters when assessing cognitive performance in patients and healthy volunteers.

Encoding Difficulty Promotes Postlearning Changes in Sleep Spindle Activity during Napping

Learning-dependent increases in sleep spindle density have been reported during nocturnal sleep immediately after the learning session. Here, we investigated experience-dependent changes in daytime sleep EEG activity after declarative learning of unrelated word pairs. At weekly intervals, 13 young male volunteers spent three 24 h sessions in the laboratory under carefully controlled homeostatic and circadian conditions. At approximately midday, subjects performed either one of two word-pair learning tasks or a matched nonlearning control task, in a counterbalanced order. The two learning lists differed in the level of concreteness of the words used, resulting in an easier and a more difficult associative encoding condition, as confirmed by performance at immediate cued recall. Subjects were then allowed to sleep for 4 h; afterward, delayed cued recall was tested. Compared with the control condition, sleep EEG spectral activity in the low spindle frequency range and the density of low-frequency sleep spindles (11.25–13.75 Hz) were both significantly increased in the left frontal cortex after the difficult but not after the easy encoding condition. Furthermore, we found positive correlations between these EEG changes during sleep and changes in memory performance between pre-nap and post-nap recall sessions. These results indicate that, like during nocturnal sleep, daytime sleep EEG oscillations including spindle activity are modified after declarative learning of word pairs. Furthermore, we demonstrate here that the nature of the learning material is a determinant factor for sleep-related alterations after declarative learning.

Homeostatic sleep pressure and responses to sustained attention in the suprachiasmatic area.

After prolonged wakefulness, people who are “night owls” do better at mental tests than those who are “early birds.” Early Birds and Night Owls In humans, peaks and troughs in alertness and cognitive performance partly depend on the timing of daily activities. Using brain imaging from the extreme ends of the spectrum of individuals whose performance is better in the mornings to those who do best in the evenings, Schmidt et al. (p. 516) found that after more than 10 hours of wakefulness, morning types had less activity in brain areas linked to attention compared with evening types. Moreover, morning types felt sleepier and tended to perform slower on psychomotor vigilance tasks. It seems getting the balance of sleep at the right time is important for regulating the daily pattern of cognitive performance. Throughout the day, cognitive performance is under the combined influence of circadian processes and homeostatic sleep pressure. Some people perform best in the morning, whereas others are more alert in the evening. These chronotypes provide a unique way to study the effects of sleep-wake regulation on the cerebral mechanisms supporting cognition. Using functional magnetic resonance imaging in extreme chronotypes, we found that maintaining attention in the evening was associated with higher activity in evening than morning chronotypes in a region of the locus coeruleus and in a suprachiasmatic area (SCA) including the circadian master clock. Activity in the SCA decreased with increasing homeostatic sleep pressure. This result shows the direct influence of the homeostatic and circadian interaction on the neural activity underpinning human behavior.

Blue Blocker Glasses as a Countermeasure for Alerting Effects of Evening Light-Emitting Diode Screen Exposure in Male Teenagers

PURPOSEnAdolescents prefer sleep and wake times that are considerably delayed compared with younger children or adults. Concomitantly, multimedia use in the evening is prevalent among teenagers and involves light exposure, particularly in the blue-wavelength range to which the biological clock and its associated arousal promotion system is the most sensitive. We investigated whether the use of blue light-blocking glasses (BB) during the evening, while sitting in front of a light-emitting diode (LED) computer screen, favors sleep initiating mechanisms at the subjective, cognitive, and physiological level.nnnMETHODSnThe ambulatory part of the study comprised 2 weeks during which the sleep-wake cycle, evening light exposure, and multimedia screen use were monitored in thirteen 15- to 17-year-old healthy male volunteers. BB or clear lenses as control glasses were worn in a counterbalanced crossover design for 1 week each, during the evening hours while using LED screens. Afterward, participants entered the laboratory and underwent an evening blue light-enriched LED screen exposure during which they wore the same glasses as during the preceding week. Salivary melatonin, subjective sleepiness, and vigilant attention were regularly assayed, and subsequent sleep was recorded by polysomnography.nnnRESULTSnCompared with clear lenses, BB significantly attenuated LED-induced melatonin suppressionxa0in the evening and decreased vigilant attention and subjective alertness before bedtime. Visually scored sleep stages and behavioral measures collected the morning after were not modified.nnnCONCLUSIONSnBB glasses may be useful in adolescents as a countermeasure for alerting effects induced by light exposure through LED screens and therefore potentially impede the negative effects modern lighting imposes on circadian physiology in the evening.

Age-related changes in sleep and circadian rhythms: impact on cognitive performance and underlying neuroanatomical networks.

Circadian and homeostatic sleep-wake regulatory processes interact in a fine tuned manner to modulate human cognitive performance. Dampening of the circadian alertness signal and attenuated deterioration of psychomotor vigilance in response to elevated sleep pressure with aging change this interaction pattern. As evidenced by neuroimaging studies, both homeostatic sleep pressure and circadian sleep-wake promotion impact on cognition-related cortical and arousal-promoting subcortical brain regions including the thalamus, the anterior hypothalamus, and the brainstem locus coeruleus (LC). However, how age-related changes in circadian and homeostatic processes impact on the cerebral activity subtending waking performance remains largely unexplored. Post-mortem studies point to neuronal degeneration in the SCN and age-related modifications in the arousal-promoting LC. Alongside, cortical frontal brain areas are particularly susceptible both to aging and misalignment between circadian and homeostatic processes. In this perspective, we summarize and discuss here the potential neuroanatomical networks underlying age-related changes in circadian and homeostatic modulation of waking performance, ranging from basic arousal to higher order cognitive behaviors.

Circadian preference modulates the neural substrate of conflict processing across the day

Human morning and evening chronotypes differ in their preferred timing for sleep and wakefulness, as well as in optimal daytime periods to cope with cognitive challenges. Recent evidence suggests that these preferences are not a simple by-product of socio-professional timing constraints, but can be driven by inter-individual differences in the expression of circadian and homeostatic sleep-wake promoting signals. Chronotypes thus constitute a unique tool to access the interplay between those processes under normally entrained day-night conditions, and to investigate how they impinge onto higher cognitive control processes. Using functional magnetic resonance imaging (fMRI), we assessed the influence of chronotype and time-of-day on conflict processing-related cerebral activity throughout a normal waking day. Sixteen morning and 15 evening types were recorded at two individually adapted time points (1.5 versus 10.5 hours spent awake) while performing the Stroop paradigm. Results show that interference-related hemodynamic responses are maintained or even increased in evening types from the subjective morning to the subjective evening in a set of brain areas playing a pivotal role in successful inhibitory functioning, whereas they decreased in morning types under the same conditions. Furthermore, during the evening hours, activity in a posterior hypothalamic region putatively involved in sleep-wake regulation correlated in a chronotype-specific manner with slow wave activity at the beginning of the night, an index of accumulated homeostatic sleep pressure. These results shed light into the cerebral mechanisms underlying inter-individual differences of higher-order cognitive state maintenance under normally entrained day-night conditions.

Dawn simulation light impacts on different cognitive domains under sleep restriction.

Chronic sleep restriction (SR) has deleterious effects on cognitive performance that can be counteracted by light exposure. However, it is still unknown if naturalistic light settings (dawn simulating light) can enhance daytime cognitive performance in a sustainable matter. Seventeen participants were enrolled in a 24-h balanced cross-over study, subsequent to SR (6-h of sleep). Two different light settings were administered each morning: a) dawn simulating light (DsL; polychromatic light gradually increasing from 0 to 250 lx during 30 min before wake-up time, with light around 250 lx for 20 min after wake-up time) and b) control dim light (DL; <8 lx). Cognitive tests were performed every 2 h during scheduled wakefulness and questionnaires were completed hourly to assess subjective mood. The analyses yielded a main effect of light condition for the motor tracking task, sustained attention to response task and a working memory task (visual 1 and 3-back task), as well as for the Simple Reaction Time Task, such that participants showed better task performance throughout the day after morning DsL exposure compared to DL. Furthermore, low performers benefited more from the light effects compared to high performers. Conversely, no significant influences from the DsL were found for the Psychomotor Vigilance Task and a contrary effect was observed for the digit symbol substitution test. No light effects were observed for subjective perception of sleepiness, mental effort, concentration and motivation. Our data indicate that short exposure to artificial morning light may significantly enhance cognitive performance in a domain-specific manner under conditions of mild SR.

Diurnal variations of hormonal secretion, alertness and cognition in extreme chronotypes under different lighting conditions

Circadian rhythms in physiology and behavior are modulated by external factors such as light or temperature. We studied whether self-selected office lighting during the habitual waking period had a different impact on alertness, cognitive performance and hormonal secretion in extreme morning and evening chronotypes (Nu2009=u200932), whose preferred bed- and wake-up times differed by several hours. The self-selected lighting condition was compared with constant bright light and a control condition in dim light. Saliva samples for hormonal analyses, subjective ratings of alertness, wellbeing, visual comfort and cognitive performance were regularly collected. Between the self-selected and the bright, but not the dim lighting condition, the onset of melatonin secretion in the evening (as marker for circadian phase) was significantly different for both chronotypes. Morning chronotypes reported a faster increase in sleepiness during the day than evening chronotypes, which was associated with higher cortisol secretion. Wellbeing, mood and performance in more difficult cognitive tasks were better in bright and self-selected lighting than in dim light for both chronotypes, whereas visual comfort was best in the self-selected lighting. To conclude, self-selection of lighting at work might positively influence biological and cognitive functions, and allow for inter-individual differences.

Sleep-Wake Regulation and Its Impact on Working Memory Performance: The Role of Adenosine

The sleep-wake cycle is regulated by a fine-tuned interplay between sleep-homeostatic and circadian mechanisms. Compelling evidence suggests that adenosine plays an important role in mediating the increase of homeostatic sleep pressure during time spent awake and its decrease during sleep. Here, we summarize evidence that adenosinergic mechanisms regulate not only the dynamic of sleep pressure, but are also implicated in the interaction of homeostatic and circadian processes. We review how this interaction becomes evident at several levels, including electrophysiological data, neuroimaging studies and behavioral observations. Regarding complex human behavior, we particularly focus on sleep-wake regulatory influences on working memory performance and underlying brain activity, with a specific emphasis on the role of adenosine in this interplay. We conclude that a change in adenosinergic mechanisms, whether exogenous or endogenous, does not only impact on sleep-homeostatic processes, but also interferes with the circadian timing system.

Sleep-dependent Neurophysiological Processes in Implicit Sequence Learning

Behavioral studies have cast doubts about the role that posttraining sleep may play in the consolidation of implicit sequence learning. Here, we used event-related fMRI to test the hypothesis that sleep-dependent functional reorganization would take place in the underlying neural circuits even in the possible absence of obvious behavioral changes. Twenty-four healthy human adults were scanned at Day 1 and then at Day 4 during an implicit probabilistic serial RT task. They either slept normally (RS) or were sleep-deprived (SD) on the first posttraining night. Unknown to them, the sequential structure of the material was based on a probabilistic finite-state grammar, with 15% chance on each trial of replacing the rules-based grammatical (G) stimulus with a nongrammatical (NG) one. Results indicated a gradual differentiation across sessions between RTs (faster RTs for G than NG), together with NG-related BOLD responses reflecting sequence learning. Similar behavioral patterns were observed in RS and SD participants at Day 4, indicating time- but not sleep-dependent consolidation of performance. Notwithstanding, we observed at Day 4 in the RS group a diminished differentiation between G- and NG-related neurophysiological responses in a set of cortical and subcortical areas previously identified as being part of the network involved in implicit sequence learning and its offline processing during sleep, indicating a sleep-dependent processing of both regular and deviant stimuli. Our results suggest the sleep-dependent development of distinct neurophysiological processes subtending consolidation of implicit motor sequence learning, even in the absence of overt behavioral differences.