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 clinician's and the researcher's attention towards the utmost importance to account for time-of-day parameters when assessing cognitive performance in patients and healthy volunteers.
BackgroundRelatively long duration retinal light exposure elicits nonvisual responses in humans, including modulation of alertness and cognition. These responses are thought to be mediated in part by melanopsin-expressing retinal ganglion cells which are more sensitive to blue light than violet or green light. The contribution of the melanopsin system and the brain mechanisms involved in the establishment of such responses to light remain to be established.Methodology/Principal FindingsWe exposed 15 participants to short duration (50 s) monochromatic violet (430 nm), blue (473 nm), and green (527 nm) light exposures of equal photon flux (1013ph/cm2/s) while they were performing a working memory task in fMRI. At light onset, blue light, as compared to green light, increased activity in the left hippocampus, left thalamus, and right amygdala. During the task, blue light, as compared to violet light, increased activity in the left middle frontal gyrus, left thalamus and a bilateral area of the brainstem consistent with activation of the locus coeruleus.Conclusion/SignificanceThese results support a prominent contribution of melanopsin-expressing retinal ganglion cells to brain responses to light within the very first seconds of an exposure. The results also demonstrate the implication of the brainstem in mediating these responses in humans and speak for a broad involvement of light in the regulation of brain function.
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.
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.
Sleep promotes memory consolidation, a process by which fresh and labile memories are reorganized into stable memories. Emotional memories are usually better remembered than neutral ones, even at long retention delays. In this study, we assessed the influence of sleep during the night after encoding onto the neural correlates of recollection of emotional memories 6 months later. After incidental encoding of emotional and neutral pictures, one-half of the subjects were allowed to sleep, whereas the others were totally sleep deprived, on the first postencoding night. During subsequent retest, functional magnetic resonance imaging sessions taking place 3 d and 6 months later, subjects made recognition memory judgments about the previously studied and new pictures. Between these retest sessions, all participants slept as usual at home. At 6 month retest, recollection was associated with significantly larger responses in subjects allowed to sleep than in sleep-deprived subjects, in the ventral medial prefrontal cortex (vMPFC) and the precuneus, two areas involved in memory retrieval, as well as in the extended amygdala and the occipital cortex, two regions the response of which was modulated by emotion at encoding. Moreover, the functional connectivity was enhanced between the vMPFC and the precuneus, as well as between the extended amygdala, the vMPFC, and the occipital cortex in the sleep group relative to the sleep-deprived group. These results suggest that sleep during the first postencoding night profoundly influences the long-term systems-level consolidation of emotional memory and modifies the functional segregation and integration associated with recollection in the long term.
The present study aimed at identifying the neurophysiological responses associated with auditory stimulation during non-rapid eye movement (NREM) sleep using simultaneous electroencephalography (EEG)/functional magnetic resonance imaging (fMRI) recordings. It was reported earlier that auditory stimuli produce bilateral activation in auditory cortex, thalamus, and caudate during both wakefulness and NREM sleep. However, due to the spontaneous membrane potential fluctuations cortical responses may be highly variable during NREM. Here we now examine the modulation of cerebral responses to tones depending on the presence or absence of sleep spindles and the phase of the slow oscillation. Thirteen healthy young subjects were scanned successfully during stage 2–4 NREM sleep in the first half of the night in a 3 T scanner. Subjects were not sleep-deprived and sounds were post hoc classified according to (i) the presence of sleep spindles or (ii) the phase of the slow oscillation during (±300 ms) tone delivery. These detected sounds were then entered as regressors of interest in fMRI analyses. Interestingly wake-like responses – although somewhat altered in size and location – persisted during NREM sleep, except during present spindles (as previously published in Dang-Vu et al., 2011) and the negative going phase of the slow oscillation during which responses became less consistent or even absent. While the phase of the slow oscillation did not alter brain responses in primary sensory cortex, it did modulate responses at higher cortical levels. In addition EEG analyses show a distinct N550 response to tones during the presence of light sleep spindles and suggest that in deep NREM sleep the brain is more responsive during the positive going slope of the slow oscillation. The presence of short temporal windows during which the brain is open to external stimuli is consistent with the fact that even during deep sleep meaningful events can be detected. Altogether, our results emphasize the notion that spontaneous fluctuations of brain activity profoundly modify brain responses to external information across all behavioral states, including deep NREM sleep.
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