The interplay between long- and short-range temporal correlations shapes cortex dynamics across vigilance states

Increasing evidence suggests that cortical dynamics during wake exhibits long-range temporal correlations suitable to integrate inputs over extended periods of time to increase the signal-to-noise ratio in decision-making and working memory tasks. Accordingly, sleep has been suggested as a state characterized by a breakdown of long-range correlations; detailed measurements of neuronal timescales that support this view, however, have so far been lacking. Here we show that the long timescales measured at the individual neuron level in freely-behaving rats during the awake state are abrogated during non-REM (NREM) sleep. We provide evidence for the existence of two distinct states in terms of timescale dynamics in cortex: one which is characterized by long timescales which dominate during wake and REM sleep, and a second one characterized by the absence of long-range temporal correlations which characterizes NREM sleep. We observe that both timescale regimes can co-exist and, in combination, lead to an apparent gradual decline of long timescales during extended wake which is restored after sleep. Our results provide a missing link between the observed long timescales in individual neuron fluctuations during wake and the reported absence of long-term correlations during deep sleep in EEG and fMRI studies. They furthermore suggest a network-level function of sleep, to reorganize cortical networks towards states governed by slow cortex dynamics to ensure optimal function for the time awake

Penguins snatch seconds-long microsleeps

Considerable research efforts have been committed to understanding the fundamental biology of sleep. Yet, this knowledge is mostly derived from laboratory studies undertaken in a handful of model organisms, such as mice, rats, and fruit flies, and in conditions that are vastly different from those where sleep evolved. Studies of nonmodel organisms in natura may help elucidate functions of sleep, but this is still largely uncharted territory and presents numerous challenges—from unconventional anatomy and physiology to distinct ecological specialization and environmental influences. On page 1026 of this issue, Libourel et al. report an unusual pattern of frequent short bouts of sleep in wild chinstrap penguins (Pygoscelis antarcticus), which calls into question not only the current understanding of how sleep architecture is regulated but also the extent to which it can be altered before the benefits of sleep are lost

Running Wheel Accessibility Affects the Regional Electroencephalogram during Sleep in Mice

Regional aspects of sleep homeostasis were investigated in mice provided with a running wheel for several weeks. Electroencephalogram (EEG) spectra of the primary motor (frontal) and somatosensory cortex (parietal) were recorded for three consecutive days. On a single day (day 2) the wheel was locked to prevent running. Wheel running correlated negatively with the frontal-parietal ratio of slow-wave activity (EEG power between 0.75 and 4.0 Hz) in the first 2 h after sleep onset (r = −0.60; P < 0.01). On day 2 frontal EEG power (2.25-8.0 Hz) in non-rapid eye movement sleep exceeded the level of the previous day, indicating that the diverse behaviors replacing wheel-running elicited more pronounced regional EEG differences. The frontal-parietal power ratio of the lower frequency bin (0.75-1.0 Hz) in the first 2 h of sleep after dark onset correlated positively with the duration of the preceding waking (r = 0.64; P < 0.001), whereas the power ratio in the remaining frequencies of the delta band (1.25-4.0 Hz) was unrelated to waking. The data suggest that in mice EEG power in the lower frequency, corresponding to the slow oscillations described in cats and humans, is related to local sleep homeostasi

Homeostatic regulation of sleep in the white-crowned sparrow (Zonotrichia leucophrys gambelii)

<p>Abstract</p> <p>Background</p> <p>Sleep is regulated by both a circadian and a homeostatic process. The homeostatic process reflects the duration of prior wakefulness: the longer one stays awake, the longer and/or more intense is subsequent sleep. In mammals, the best marker of the homeostatic sleep drive is slow wave activity (SWA), the electroencephalographic (EEG) power spectrum in the 0.5–4 Hz frequency range during non-rapid eye movement (NREM) sleep. In mammals, NREM sleep SWA is high at sleep onset, when sleep pressure is high, and decreases progressively to reach low levels in late sleep. Moreover, SWA increases further with sleep deprivation, when sleep also becomes less fragmented (the duration of sleep episodes increases, and the number of brief awakenings decreases). Although avian and mammalian sleep share several features, the evidence of a clear homeostatic response to sleep loss has been conflicting in the few avian species studied so far. The aim of the current study was therefore to ascertain whether established markers of sleep homeostasis in mammals are also present in the white-crowned sparrow (<it>Zonotrichia leucophrys gambelii</it>), a migratory songbird of the order Passeriformes. To accomplish this goal, we investigated amount of sleep, sleep time course, and measures of sleep intensity in 6 birds during baseline sleep and during recovery sleep following 6 hours of sleep deprivation.</p> <p>Results</p> <p>Continuous (24 hours) EEG and video recordings were used to measure baseline sleep and recovery sleep following short-term sleep deprivation. Sleep stages were scored visually based on 4-sec epochs. EEG power spectra (0.5–25 Hz) were calculated on consecutive 4-sec epochs. Four vigilance states were reliably distinguished based on behavior, visual inspection of the EEG, and spectral EEG analysis: Wakefulness (W), Drowsiness (D), slow wave sleep (SWS) and rapid-eye movement (REM) sleep. During baseline, SWA during D, SWS, and NREM sleep (defined as D and SWS combined) was highest at the beginning of the major sleep period and declined thereafter. Moreover, peak SWA in both SWS and NREM sleep increased significantly immediately following sleep deprivation relative to baseline.</p> <p>Conclusion</p> <p>As in mammals, sleep deprivation in the white-crowned sparrow increases the intensity of sleep as measured by SWA.</p

Sleep in Kcna2 knockout mice

<p>Abstract</p> <p>Background</p> <p><it>Shaker </it>codes for a <it>Drosophila </it>voltage-dependent potassium channel. Flies carrying <it>Shaker </it>null or hypomorphic mutations sleep 3–4 h/day instead of 8–14 h/day as their wild-type siblings do. Shaker-like channels are conserved across species but it is unknown whether they affect sleep in mammals. To address this issue, we studied sleep in <it>Kcna2 </it>knockout (KO) mice. <it>Kcna2 </it>codes for Kv1.2, the alpha subunit of a Shaker-like voltage-dependent potassium channel with high expression in the mammalian thalamocortical system.</p> <p>Results</p> <p>Continuous (24 h) electroencephalograph (EEG), electromyogram (EMG), and video recordings were used to measure sleep and waking in <it>Kcna2 </it>KO, heterozygous (HZ) and wild-type (WT) pups (P17) and HZ and WT adult mice (P67). Sleep stages were scored visually based on 4-s epochs. EEG power spectra (0–20 Hz) were calculated on consecutive 4-s epochs. KO pups die by P28 due to generalized seizures. At P17 seizures are either absent or very rare in KO pups (< 1% of the 24-h recording time), and abnormal EEG activity is only present during the seizure. KO pups have significantly less non-rapid eye movement (NREM) sleep (-23%) and significantly more waking (+21%) than HZ and WT siblings with no change in rapid eye movement (REM) sleep time. The decrease in NREM sleep is due to an increase in the number of waking episodes, with no change in number or duration of sleep episodes. Sleep patterns, daily amounts of sleep and waking, and the response to 6 h sleep deprivation are similar in HZ and WT adult mice.</p> <p>Conclusion</p> <p>Kv1.2, a mammalian homologue of Shaker, regulates neuronal excitability and affects NREM sleep.</p

Environment shapes sleep patterns in a wild nocturnal primate

Among primates, the suborder Haplorhini is considered to have evolved a consolidated monophasic sleep pattern, with diurnal species requiring a shorter sleep duration than nocturnal species. Only a few primate species have been systematically studied in their natural habitat where environmental variables, including temperature and light, have a major influence on sleep and activity patterns. Here we report the first sleep study on a nocturnal primate performed in the wild. We fitted seven wild Javan slow lorises (Nycticebus javanicus) in West Java, Indonesia with accelerometers that collected activity data, and installed climate loggers in each individual's home range to collect ambient temperature readings (over 321 days in total). All individuals showed a strictly nocturnal pattern of activity and displayed a striking synchronisation of onset and cessation of activity in relation to sunset and sunrise. The longest consolidated rest episodes were typically clustered near the beginning and towards the end of the light period, and this pattern was inversely related to daily fluctuations of the ambient temperature. The striking relationship between daily activity patterns, light levels and temperature suggests a major role of the environment in shaping the daily architecture of waking and sleep. We concluded that well-known phenotypic variability in daily sleep amount and architecture across species may represent an adaptation to changes in the environment. Our data suggest that the consolidated monophasic sleep patterns shaped by environmental pressures observed in slow lorises represent phylogenetic inertia in the evolution of sleep patterns in humans

Neuronal-spiking-based closed-loop stimulation during cortical ON- and OFF-states in freely moving mice.

The slow oscillation is a central neuronal dynamic during sleep, and is generated by alternating periods of high and low neuronal activity (ON- and OFF-states). Mounting evidence causally links the slow oscillation to sleep's functions, and it has recently become possible to manipulate the slow oscillation non-invasively and phase-specifically. These developments represent promising clinical avenues, but they also highlight the importance of improving our understanding of how ON/OFF-states affect incoming stimuli and what role they play in neuronal plasticity. Most studies using closed-loop stimulation rely on the electroencephalogram and local field potential signals, which reflect neuronal ON- and OFF-states only indirectly. Here we develop an online detection algorithm based on spiking activity recorded from laminar arrays in mouse motor cortex. We find that online detection of ON- and OFF-states reflects specific phases of spontaneous local field potential slow oscillation. Our neuronal-spiking-based closed-loop procedure offers a novel opportunity for testing the functional role of slow oscillation in sleep-related restorative processes and neural plasticity

Psilocin acutely alters sleep-wake architecture and cortical brain activity in laboratory mice

Serotonergic psychedelic drugs, such as psilocin (4-hydroxy-N,N-dimethyltryptamine), profoundly alter the quality of consciousness through mechanisms which are incompletely understood. Growing evidence suggests that a single psychedelic experience can positively impact long-term psychological well-being, with relevance for the treatment of psychiatric disorders, including depression. A prominent factor associated with psychiatric disorders is disturbed sleep, and the sleep-wake cycle is implicated in the homeostatic regulation of neuronal activity and synaptic plasticity. However, it remains largely unknown to what extent psychedelic agents directly affect sleep, in terms of both acute arousal and homeostatic sleep regulation. Here, chronic electrophysiological recordings were obtained in mice to track sleep-wake architecture and cortical activity after psilocin injection. Administration of psilocin led to delayed REM sleep onset and reduced NREM sleep maintenance for up to approximately 3 h after dosing, and the acute EEG response was associated primarily with an enhanced oscillation around 4 Hz. No long-term changes in sleep-wake quantity were found. When combined with sleep deprivation, psilocin did not alter the dynamics of homeostatic sleep rebound during the subsequent recovery period, as reflected in both sleep amount and EEG slow-wave activity. However, psilocin decreased the recovery rate of sleep slow-wave activity following sleep deprivation in the local field potentials of electrodes targeting the medial prefrontal and surrounding cortex. It is concluded that psilocin affects both global vigilance state control and local sleep homeostasis, an effect which may be relevant for its antidepressant efficacy

Environment shapes sleep patterns in a wild nocturnal primate

Among primates, the suborder Haplorhini is considered to have evolved a consolidated monophasic sleep pattern, with diurnal species requiring a shorter sleep duration than nocturnal species. Only a few primate species have been systematically studied in their natural habitat where environmental variables, including temperature and light, have a major influence on sleep and activity patterns. Here we report the first sleep study on a nocturnal primate performed in the wild. We fitted seven wild Javan slow lorises (Nycticebus javanicus) in West Java, Indonesia with accelerometers that collected activity data, and installed climate loggers in each individual’s home range to collect ambient temperature readings (over 321 days in total). All individuals showed a strictly nocturnal pattern of activity and displayed a striking synchronisation of onset and cessation of activity in relation to sunset and sunrise. The longest consolidated rest episodes were typically clustered near the beginning and towards the end of the light period, and this pattern was inversely related to daily fluctuations of the ambient temperature. The striking relationship between daily activity patterns, light levels and temperature suggests a major role of the environment in shaping the daily architecture of waking and sleep. We concluded that well-known phenotypic variability in daily sleep amount and architecture across species may represent an adaptation to changes in the environment. Our data suggest that the consolidated monophasic sleep patterns shaped by environmental pressures observed in slow lorises represent phylogenetic inertia in the evolution of sleep patterns in humans

Sleep homeostasis during daytime food entrainment in mice

24h rhythms of physiology and behavior are driven by the environment and an internal endogenous timing system. Daily restricted feeding (RF) in nocturnal rodents during their inactive phase initiates food anticipatory activity (FAA) and a reorganisation of the typical 24h sleep-wake structure. Here, we investigate the effects of daytime feeding, where food access was restricted to 4h during the light period ZT4-8 (Zeitgeber time; ZT0 is lights on), on sleep-wake architecture and sleep homeostasis in mice. Following 10 days of RF, mice were returned to ad libitum feeding. To mimic the spontaneous wakefulness associated with FAA and daytime feeding, mice were then sleep deprived between ZT3-6. While the amount of wake increased during FAA and subsequent feeding, total wake time over 24h remained stable as the loss of sleep in the light phase was compensated for by an increase in sleep in the dark phase. Interestingly, sleep which followed spontaneous wake episodes during the dark period and the extended period of wake associated with FAA, exhibited lower levels of slow-wave activity (SWA) when compared to baseline or after sleep deprivation, despite a similar duration of waking. This suggests an evolutionary mechanism of reducing sleep drive during negative energy balance to enable greater arousal for food seeking behaviors. However, the total amount of sleep and SWA accumulated during the 24h was similar between baseline and RF. In summary, our study suggests that despite substantial changes in the daily distribution and quality of wake induced by RF, sleep homeostasis is maintained.</p