Homeostatic regulation of sleep in arrhythmic Siberian hamsters

2004 ◽  
Vol 287 (1) ◽  
pp. R104-R111 ◽  
Author(s):  
Jennie E. Larkin ◽  
Tohei Yokogawa ◽  
H. Craig Heller ◽  
Paul Franken ◽  
Norman F. Ruby

Sleep is regulated by independent yet interacting circadian and homeostatic processes. The present study used a novel approach to study sleep homeostasis in the absence of circadian influences by exposing Siberian hamsters to a simple phase delay of the photocycle to make them arrhythmic. Because these hamsters lacked any circadian organization, their sleep homeostasis could be studied in the absence of circadian interactions. Control animals retained circadian rhythmicity after the phase shift and re-entrained to the phase-shifted photocycle. These animals displayed robust daily sleep-wake rhythms with consolidated sleep during the light phase beginning about 1 h after light onset. This marked sleep-wake pattern was circadian in that it persisted in constant darkness. The distribution of sleep in the arrhythmic hamsters over 24 h was similar to that in the light phase of rhythmic animals. Therefore, daily sleep amounts were higher in arrhythmic animals compared with rhythmic ones. During 2- and 6-h sleep deprivations (SD), it was more difficult to keep arrhythmic hamsters awake than it was for rhythmic hamsters. Because the arrhythmic animals obtained more non-rapid eye movement sleep (NREMS) during the SD, they showed a diminished compensatory response in NREMS EEG slow-wave activity during recovery sleep. When amounts of sleep during the SD were taken into account, there were no differences in sleep homeostasis between experimental and control hamsters. Thus loss of circadian control did not alter the homeostatic response to SD. This supports the view that circadian and homeostatic influences on sleep regulation are independent processes.

2017 ◽  
Vol 117 (1) ◽  
pp. 327-335 ◽  
Author(s):  
Irma Gvilia ◽  
Natalia Suntsova ◽  
Andrey Kostin ◽  
Anna Kalinchuk ◽  
Dennis McGinty ◽  
...  

Sleep homeostasis in rats undergoes significant maturational changes during postweaning development, but the underlying mechanisms of this process are unknown. In the present study we tested the hypothesis that the maturation of sleep is related to the functional emergence of adenosine (AD) signaling in the brain. We assessed postweaning changes in 1) wake-related elevation of extracellular AD in the basal forebrain (BF) and adjacent lateral preoptic area (LPO), and 2) the responsiveness of median preoptic nucleus (MnPO) sleep-active cells to increasing homeostatic sleep drive. We tested the ability of exogenous AD to augment homeostatic responses to sleep deprivation (SD) in newly weaned rats. In groups of postnatal day (P)22 and P30 rats, we collected dialysate from the BF/LPO during baseline (BSL) wake-sleep, SD, and recovery sleep (RS). HPLC analysis of microdialysis samples revealed that SD in P30 rats results in significant increases in AD levels compared with BSL. P22 rats do not exhibit changes in AD levels in response to SD. We recorded neuronal activity in the MnPO during BSL, SD, and RS at P22/P30. MnPO neurons exhibited adult-like increases in waking neuronal discharge across SD on both P22 and P30, but discharge rates during enforced wake were higher on P30 vs. P22. Central administration of AD (1 nmol) during SD on P22 resulted in increased sleep time and EEG slow-wave activity during RS compared with saline control. Collectively, these findings support the hypothesis that functional reorganization of an adenosinergic mechanism of sleep regulation contributes to the maturation of sleep homeostasis. NEW & NOTEWORTHY Brain mechanisms that regulate the maturation of sleep are understudied. The present study generated first evidence about a potential mechanistic role for adenosine in the maturation of sleep homeostasis. Specifically, we demonstrate that early postweaning development in rats, when homeostatic response to sleep loss become adult like, is characterized by maturational changes in wake-related production/release of adenosine in the brain. Pharmacologically increased adenosine signaling in developing brain facilitates homeostatic responses to sleep deprivation.


1998 ◽  
Vol 274 (4) ◽  
pp. R1186-R1194 ◽  
Author(s):  
Takuro Endo ◽  
Corinne Roth ◽  
Hans-Peter Landolt ◽  
Esther Werth ◽  
Daniel Aeschbach ◽  
...  

To investigate rapid eye movement (REM) sleep regulation, eight healthy young men were deprived of REM sleep for three consecutive nights. In a three-night control sleep deprivation (CD) session 2 wk later, the subjects were repeatedly awakened from non-REM sleep in an attempt to match the awakenings during the REM sleep deprivation (RD) nights. During the RD nights the number of sleep interruptions required to prevent REM sleep increased within and across consecutive nights. REM sleep was reduced to 9.2% of baseline (CD nights: 80.7%) and rose to 140.1% in the first recovery night. RD gave rise to changes in the EEG power spectra of REM sleep. Power in the 8.25- to 11-Hz range was reduced in the first recovery night, an effect that gradually subsided but was still present in the third recovery night. The rising REM sleep propensity, as reflected by the increase of interventions within and across RD nights, and the moderate REM sleep rebound during recovery can be accounted for by a compensatory response that serves REM sleep homeostasis. The changes in the electroencephalogram power spectra, which were observed during enhanced REM sleep propensity, may be a sign of an altered quality of REM sleep.


SLEEP ◽  
2021 ◽  
Author(s):  
Jelena Skorucak ◽  
Nathan Weber ◽  
Mary A Carskadon ◽  
Chelsea Reynolds ◽  
Scott Coussens ◽  
...  

Abstract The high prevalence of chronic sleep restriction in adolescents underscores the importance of understanding how adolescent sleep is regulated under such conditions. One component of sleep regulation is a homeostatic process: if sleep is restricted, then sleep intensity increases. Our knowledge of this process is primarily informed by total sleep deprivation studies and has been incorporated in mathematical models of human sleep regulation. Several animal studies, however, suggest that adaptation occurs in chronic sleep restriction conditions, showing an attenuated or even decreased homeostatic response. We investigated the homeostatic response of adolescents to different sleep opportunities. Thirty-four participants were allocated to one of three groups with 5, 7.5 or 10 h of sleep opportunity per night for 5 nights. Each group underwent a protocol of 9 nights designed to mimic a school week between 2 weekends: 2 baseline nights (10 h sleep opportunity), 5 condition nights (5, 7.5 or 10 h), and two recovery nights (10 h). Measures of sleep homeostasis (slow-wave activity and slow-wave energy) were calculated from frontal and central EEG derivations and compared to predictions derived from simulations of the homeostatic process of the two-process model of sleep regulation. Only minor differences were found between empirical data and model predictions, indicating that sleep homeostasis is preserved under chronic sleep restriction in adolescents. These findings improve our understanding of effects of repetitive short sleep in adolescents.


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.


1965 ◽  
Vol s3-106 (76) ◽  
pp. 315-325
Author(s):  
A. C. NEVILLE

A circadian clock is shown to be involved in the control of macromolecular orientation of chitin by cells secreting and organizing insect endocuticle. Daily organization of locust endocuticle into alternating lamellate and non-lamellate layers persists in constant temperature (36° C) and constant darkness for at least 2 weeks; the freerunning period is then about 23 h, so that after a number of days the circadian clock is 180° out of phase with the astronomical clock, with which it is normally phased. The rhythm is almost independent of temperature, with a Q10 of 1.04, as contrasted with a Q10 of 2.0 for the actual rate of increase of endocuticular thickness. Locust epidermal cells differ in response to specific imposed environmental conditions according to their location in the integument. In some cells, constant low temperature uncouples chitin lamellogenesis from the circadian clock, provided that illumination (light or dark) is constant also: the result is continuously lamellate endocuticle. In other cells constant light acts as an uncoupling factor, provided that temperature (high or low) is constant also: the result in this case is continuously non-lamellate endocuticle. The circadian rhythm of chitin lamellogenesis persists in a cave cricket (Dolichopoda linderi). A similar circadian lamellogenesis rhythm occurs in the endocuticle of nymphs and adults of the cockroach Periplaneta americana. A crossed-fibre multiple-ply endocuticle in the legs and wings of giant toe-biter water bugs (Belosto-matidae) also displays circadian organization, the chitin macromolecules in any one layer lying in parallel fibres, at an angle of approximately 6o° to those in the next layer. It is suggested that daily organization of the skeleton may be a general feature of arthropods. Examples include the phenomena of timing of chitin lamellogenesis; chitin crossed-fibrillar organization; degree of fluorescence of the rubber-like protein resilin; and mineralization of crayfish gastroliths.


2003 ◽  
Vol 285 (2) ◽  
pp. R413-R419 ◽  
Author(s):  
Paul Franken ◽  
Phung Gip ◽  
Grace Hagiwara ◽  
Norman F. Ruby ◽  
H. Craig Heller

Sleep has been functionally implicated in brain energy homeostasis in that it could serve to replenish brain energy stores that become depleted while awake. Sleep deprivation (SD) should therefore lower brain glycogen content. We tested this hypothesis by sleep depriving mice of three inbred strains, i.e., AKR/J (AK), DBA/2J (D2), and C57BL/6J (B6), that differ greatly in their sleep regulation. After a 6-h SD, these mice and their controls were killed by microwave irradiation, and glycogen and glucose were quantified in the cerebral cortex, brain stem, and cerebellum. After SD, both measures significantly increased by ∼40% in the cortex of B6 mice, while glycogen significantly decreased by 20–38% in brain stem and cerebellum of AK and D2 mice. In contrast, after SD, glucose content increased in all three structures in AK mice and did not change in D2 mice. The increase in glycogen after SD in B6 mice persisted under conditions of food deprivation that, by itself, lowered cortical glycogen. Furthermore, the strains that differ most in their compensatory response to sleep loss, i.e., AK and D2, did not differ in their glycogen response. Thus glycogen content per se is an unlikely end point of sleep's functional role in brain energy homeostasis.


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.


Author(s):  
Cassie J. Hilditch ◽  
Erin E. Flynn-Evans

This chapter examines circadian rhythms and homeostatic mechanisms for sleep regulation. It reviews the current evidence describing the two-process model of sleep regulation and how to assess disruption to either of these sleep drives. This chapter also reviews the role of the photic and non-photic resetting of the circadian rhythm and describes how some aspects of modern society can cause sleep and circadian disruption. Further, this chapter describes how misalignment between the circadian rhythm and sleep homeostasis, such as occurs during jet lag and shift-work, can lead to sleep disruption. The short- and long-term consequences of circadian misalignment are also reviewed.


1985 ◽  
Vol 248 (4) ◽  
pp. R434-R438 ◽  
Author(s):  
H. E. Albers ◽  
L. Yogev ◽  
R. B. Todd ◽  
B. D. Goldman

The 24-h patterns of circulating cortisol and corticosterone were determined in male hamsters housed under a 14:10 light-dark cycle. Corticoid levels varied significantly over the 24-h sampling period with peak levels of both hormones occurring near the onset of the daily dark phase. The ratio of cortisol to corticosterone changed dramatically during the day. Corticosterone levels were significantly higher than cortisol during the early part of the light phase; however, cortisol levels became significantly higher than corticosterone when both hormones began their daily rise. To examine whether the circadian rhythm of cortisol secretion could be involved in the physiological control of hamster circadian organization, cortisol was infused at approximately physiological levels into adrenalectomized hamsters either continuously or in a 24-h rhythm. No significant differences were observed in the timing of circadian wheel-running rhythms in hamsters housed in LD 16:8, LD 14:10, or LL when cortisol was infused continuously, in a 24-h rhythm that mimicked the cortisol rhythm of intact hamsters, or in a 24-h rhythm several hours out of phase with the rhythm of intact hamsters. Provision of cortisol in a 24-h rhythm appeared to promote the survival of adrenalectomized hamsters since hamsters receiving a 24-h pattern of cortisol survived the experimental protocol significantly longer than those receiving the same dose of cortisol continuously.


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