Loss of circadian organization of sleep and wakefulness during hibernation

2002 ◽  
Vol 282 (4) ◽  
pp. R1086-R1095 ◽  
Author(s):  
Jennie E. Larkin ◽  
Paul Franken ◽  
H. Craig Heller

We investigated circadian and homeostatic regulation of nonrapid eye movement (NREM) sleep in golden-mantled ground squirrels during euthermic intervals between torpor bouts. Slow-wave activity (SWA; 1–4 Hz) and sigma activity (10–15 Hz) represent the two dominant electroencephalographic (EEG) frequency components of NREM sleep. EEG sigma activity has a strong circadian component in addition to a sleep homeostatic component, whereas SWA mainly reflects sleep homeostasis [Dijk DJ and Czeisler CA. J Neurosci 15: 3526–3538, 1995; Dijk DJ, Shanahan TL, Duffy JF, Ronda JM, and Czeisler CA. J Physiol (Lond) 505: 851–858, 1997]. Animals maintained under constant conditions continued to display circadian rhythms in both sigma activity and brain temperature throughout euthermic intervals, whereas sleep and wakefulness showed no circadian organization. Instead, sleep and wakefulness were distributed according to a 6-h ultradian rhythm. SWA, NREM sleep bout length, and sigma activity responded homeostatically to the ultradian sleep-wake pattern. We suggest that the loss of sleep-wake consolidation in ground squirrels during the hibernation season may be related to the greatly decreased locomotor activity during the hibernation season and may be necessary for maintenance of multiday torpor bouts characteristic of hibernating species.

1999 ◽  
Vol 276 (2) ◽  
pp. R522-R529 ◽  
Author(s):  
Jennie E. Larkin ◽  
H. Craig Heller

Electroencephalographic slow-wave activity (SWA) in non-rapid eye movement (NREM) sleep is directly related to prior sleep/wake history, with high levels of SWA following extended periods of wake. Therefore, SWA has been thought to reflect the level of accumulated sleep need. The discovery that euthermic intervals between hibernation bouts are spent primarily in sleep and that this sleep is characterized by high and monotonically declining SWA has led to speculation that sleep homeostasis may play a fundamental role in the regulation of the timing of bouts of hibernation and periodic arousals to euthermia. It was proposed that because the SWA profile seen after arousal from hibernation is strikingly similar to what is seen in nonhibernating mammals after extended periods of wakefulness, that hibernating mammals may arouse from hibernation with significant accumulated sleep need. This sleep need may accumulate during hibernation because the low brain temperatures during hibernation may not be compatible with sleep restorative processes. In the present study, golden-mantled ground squirrels were sleep deprived during the first 4 h of interbout euthermia by injection of caffeine (20 mg/kg ip). We predicted that if the SWA peaks after bouts of hibernation reflected a homeostatic response to an accumulated sleep need, sleep deprivation should simply have displaced and possibly augmented the SWA to subsequent recovery sleep. Instead we found that after caffeine-induced sleep deprivation of animals just aroused from hibernation, the anticipated high SWA typical of recovery sleep did not occur. Similar results were found in a study that induced sleep deprivation by gentle handling (19). These findings indicate that the SWA peak immediately after hibernation does not represent homeostatic regulation of NREM sleep, as it normally does after prolonged wakefulness during euthermia, but instead may reflect some other neurological process in the recovery of brain function from an extended period at low temperature.


1996 ◽  
Vol 270 (4) ◽  
pp. R777-R784 ◽  
Author(s):  
J. E. Larkin ◽  
H. C. Heller

Brain temperature (Tbr), vigilance state, and electroencephalograph slow-wave activity (EEG SWA, 1.0-4.0 Hz) were measured during hibernation and spontaneous arousals to euthermia in seven golden-mantled ground squirrels (Spermophilus lateralis). Animals were held at air temperatures (Ta) ranging from 6 to 21 degrees C. SWA was used as a measure of the intensity of non-rapid eye movement (NREM) sleep. Squirrels that had hibernated at high Ta had lower SWA in NREM sleep in the hours following arousal than when they hibernated at low Ta. SWA in NREM sleep during euthermia immediately following arousal was significantly correlated to minimum Tbr and SWA during hibernation. The duration of the preceding hibernation bout had no significant effect on SWA during euthermia. We hypothesize that the restorative process of sleep, reflected by SWA, is temperature sensitive and is compromised by the low temperatures in hibernation. The accumulation of a SWA debt during hibernation may be related to the temperature-dependent depression of SWA during hibernation.


2020 ◽  
Author(s):  
Maria H Eriksson ◽  
Torsten Baldeweg ◽  
Ronit Pressler ◽  
Stewart G Boyd ◽  
Reto Huber ◽  
...  

AbstractObjectiveSleep disruption and cognitive impairment are important co-morbidities in childhood epilepsy, yet a mechanistic link has not been substantiated. Slow wave activity during sleep and its homeostatic decrease across the night is associated with synaptic renormalisation, and shows maturational changes over the course of childhood. Here, we aimed to investigate the effect of epilepsy on sleep homeostasis in the developing brain.MethodsWe examined the relationship of sleep homeostasis as reflected in slow wave activity to seizures, cognition and behaviour, comparing 22 children (aged 6 to 16 years) with focal epilepsy to 21 age-matched healthy controls. Participants underwent overnight sleep EEG and IQ testing and performed memory consolidation tasks. Their parents completed standard behavioural questionnaires.ResultsChildren with epilepsy had lower slow wave activity at the start of non-rapid eye movement (NREM) sleep, though similar overnight decline and slow wave activity in the final hour of NREM sleep. Both groups displayed an antero-posterior shift in peak slow wave activity overnight, though individual patients showed persistent local increases at scalp locations matching those of focal interictal discharges. Patients who had seizures during their admission had lower early-night slow wave activity, the group without seizures showing similar activity to controls. We found a positive correlation between full scale IQ and early-night slow wave activity in patients but not controls.InterpretationReduced early night slow wave activity in children with focal epilepsies is correlated with lower cognitive ability and more seizures and may reflect a reduction in learning-related synaptic potentiation.


1996 ◽  
Vol 271 (5) ◽  
pp. R1364-R1371 ◽  
Author(s):  
T. Deboer ◽  
I. Tobler

Sleep, daily torpor, and hibernation have been considered to be homologous processes. However, in the Djungarian hamster, daily torpor is followed by an increase in slow-wave activity (SWA; electroencephalogram power density 0.75-4.0 Hz) that is similar to the increase observed after sleep deprivation. A positive correlation was found between torpor episode length and the subsequent increase in SWA, which was highest when SWA was assumed to increase with a saturating exponential function. Thus the increase in SWA propensity during daily torpor followed similar kinetics as during waking, supporting the hypothesis that when the animal is in torpor it is incurring a sleep debt. An alternative hypothesis, proposing that the mode of arousal causes the subsequent SWA increase, was tested by warming the animals during emergence from daily torpor. Irrespective of mode of arousal, more non-rapid eye movement (NREM) sleep and a similar SWA increase was found after torpor. The data are compatible with a putative neuronal restorative function for sleep associated with the expression of SWA in NREM sleep. During torpor, when brain temperature is low, this function is inhibited, whereas the need for restoration accumulates. Recovery takes place only after return to euthermia.


2005 ◽  
Vol 289 (3) ◽  
pp. R827-R838 ◽  
Author(s):  
F. C. Baker ◽  
C. Angara ◽  
R. Szymusiak ◽  
D. McGinty

The suprachiasmatic nucleus (SCN) regulates the circadian rhythms of body temperature (Tb) and vigilance states in mammals. We studied rats in which circadian rhythmicity was abolished after SCN lesions (SCNx rats) to investigate the association between the ultradian rhythms of sleep-wake states and brain temperature (Tbr), which are exposed after lesions. Ultradian rhythms of Tbr (mean period: 3.6 h) and sleep were closely associated in SCNx rats. Within each ultradian cycle, nonrapid eye movement (NREM) sleep was initiated 5 ± 1 min after Tbr peaks, after which temperature continued a slow decline (0.02 ± 0.006°C/min) until it reached a minimum. Sleep and slow wave activity (SWA), an index of sleep intensity, were associated with declining temperature. Cross-correlation analysis revealed that the rhythm of Tbr preceded that of SWA by 2–10 min. We also investigated the thermoregulatory and sleep-wake responses of SCNx rats and controls to mild ambient cooling (18°C) and warming (30°C) over 24-h periods. SCNx rats and controls responded similarly to changes in ambient temperature. Cooling decreased REM sleep and increased wake. Warming increased Tbr, blunted the amplitude of ultradian Tbr rhythms, and increased the number of transitions into NREM sleep. SCNx rats and controls had similar percentages of NREM sleep, REM sleep, and wake, as well as the same average Tb within each 24-h period. Our results suggest that, in rats, the SCN modulates the timing but not the amount of sleep or the homeostatic control of sleep-wake states or Tb during deviations in ambient temperature.


Author(s):  
Christopher B O'Brien ◽  
Clarence E Locklear ◽  
Zachary T Glovak ◽  
Diana Zebadúa Unzaga ◽  
Helen A Baghdoyan ◽  
...  

The electroencephalogram (EEG) provides an objective, neural correlate of consciousness. Opioid receptors modulate mammalian neuronal excitability, and this fact was used to characterize how opioids administered to mice alter EEG power and states of consciousness. The present study tested the hypothesis that antinociceptive doses of fentanyl, morphine, or buprenorphine differentially alter the EEG and states of sleep and wakefulness in adult, male C57BL/6J mice. Mice were anesthetized and implanted with telemeters that enabled wireless recordings of cortical EEG and electromyogram (EMG). After surgical recovery, EEG and EMG were used to objectively score states of consciousness as wakefulness, rapid eye movement (REM) sleep, or non-REM (NREM) sleep. Measures of EEG power (dB) were quantified as delta (0.5 to 4 Hz), theta (4 to 8 Hz), alpha (8 to 13 Hz), sigma (12 to 15 Hz), beta (13 to 30 Hz), and gamma (30 to 60 Hz). Compared to saline (control), fentanyl and morphine decreased NREM sleep, morphine eliminated REM sleep, and buprenorphine eliminated NREM sleep and REM sleep. Opioids significantly and differentially disrupted the temporal organization of sleep/wake states, altered specific EEG frequency bands, and caused dissociated states of consciousness. The results are discussed relative to the fact that opioids, pain, and sleep modulate interacting states of consciousness.


2017 ◽  
Vol 40 ◽  
pp. e115-e116
Author(s):  
M. Gorgoni ◽  
F. Reda ◽  
G. Lauri ◽  
I. Truglia ◽  
S. Cordone ◽  
...  

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Christopher W Thomas ◽  
Mathilde CC Guillaumin ◽  
Laura E McKillop ◽  
Peter Achermann ◽  
Vladyslav V Vyazovskiy

Sleep homeostasis manifests as a relative constancy of its daily amount and intensity. Theoretical descriptions define ‘Process S’, a variable with dynamics dependent on global sleep-wake history, and reflected in electroencephalogram (EEG) slow wave activity (SWA, 0.5–4 Hz) during sleep. The notion of sleep as a local, activity-dependent process suggests that activity history must be integrated to determine the dynamics of global Process S. Here, we developed novel mathematical models of Process S based on cortical activity recorded in freely behaving mice, describing local Process S as a function of the deviation of neuronal firing rates from a locally defined set-point, independent of global sleep-wake state. Averaging locally derived Processes S and their rate parameters yielded values resembling those obtained from EEG SWA and global vigilance states. We conclude that local Process S dynamics reflects neuronal activity integrated over time, and global Process S reflects local processes integrated over space.


2017 ◽  
pp. 55-77 ◽  
Author(s):  
James T. McKenna ◽  
Mark R. Zielinski ◽  
Robert W. McCarley

SLEEP ◽  
2019 ◽  
Vol 43 (6) ◽  
Author(s):  
Sjoerd J van Hasselt ◽  
Maria Rusche ◽  
Alexei L Vyssotski ◽  
Simon Verhulst ◽  
Niels C Rattenborg ◽  
...  

Abstract Most of our knowledge about the regulation and function of sleep is based on studies in a restricted number of mammalian species, particularly nocturnal rodents. Hence, there is still much to learn from comparative studies in other species. Birds are interesting because they appear to share key aspects of sleep with mammals, including the presence of two different forms of sleep, i.e. non-rapid eye movement (NREM) and rapid eye movement (REM) sleep. We examined sleep architecture and sleep homeostasis in the European starling, using miniature dataloggers for electroencephalogram (EEG) recordings. Under controlled laboratory conditions with a 12:12 h light–dark cycle, the birds displayed a pronounced daily rhythm in sleep and wakefulness with most sleep occurring during the dark phase. Sleep mainly consisted of NREM sleep. In fact, the amount of REM sleep added up to only 1~2% of total sleep time. Animals were subjected to 4 or 8 h sleep deprivation to assess sleep homeostatic responses. Sleep deprivation induced changes in subsequent NREM sleep EEG spectral qualities for several hours, with increased spectral power from 1.17 Hz up to at least 25 Hz. In contrast, power below 1.17 Hz was decreased after sleep deprivation. Sleep deprivation also resulted in a small compensatory increase in NREM sleep time the next day. Changes in EEG spectral power and sleep time were largely similar after 4 and 8 h sleep deprivation. REM sleep was not noticeably compensated after sleep deprivation. In conclusion, starlings display signs of NREM sleep homeostasis but the results do not support the notion of important REM sleep functions.


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