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Loss of Gnas imprinting differentially affects REM/NREM sleep and cognition in mice.

ABSTRACT: It has been suggested that imprinted genes are important in the regulation of sleep. However, the fundamental question of whether genomic imprinting has a role in sleep has remained elusive up to now. In this work we show that REM and NREM sleep states are differentially modulated by the maternally expressed imprinted gene Gnas. In particular, in mice with loss of imprinting of Gnas, NREM and complex cognitive processes are enhanced while REM and REM-linked behaviors are inhibited. This is the first demonstration that a specific overexpression of an imprinted gene affects sleep states and related complex behavioral traits. Furthermore, in parallel to the Gnas overexpression, we have observed an overexpression of Ucp1 in interscapular brown adipose tissue (BAT) and a significant increase in thermoregulation that may account for the REM/NREM sleep phenotypes. We conclude that there must be significant evolutionary advantages in the monoallelic expression of Gnas for REM sleep and for the consolidation of REM-dependent memories. Conversely, biallelic expression of Gnas reinforces slow wave activity in NREM sleep, and this results in a reduction of uncertainty in temporal decision-making processes.

SUBMITTER: Lassi G

PROVIDER: S-EPMC3349741 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Loss of Gnas imprinting differentially affects REM/NREM sleep and cognition in mice.

Lassi Glenda G Ball Simon T ST Maggi Silvia S Colonna Giovanni G Nieus Thierry T Cero Cheryl C Bartolomucci Alessandro A Peters Jo J Tucci Valter V

PLoS genetics 20120510 5

It has been suggested that imprinted genes are important in the regulation of sleep. However, the fundamental question of whether genomic imprinting has a role in sleep has remained elusive up to now. In this work we show that REM and NREM sleep states are differentially modulated by the maternally expressed imprinted gene Gnas. In particular, in mice with loss of imprinting of Gnas, NREM and complex cognitive processes are enhanced while REM and REM-linked behaviors are inhibited. This is the f ...[more]

PMID: 22589743

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Project description:We previously demonstrated that seizure occurrences at different zeitgeber times alter sleep and circadian rhythm differently. On the other hand, the synchronized delta wave of electroencephalogram (EEG) during non-rapid eye movement (NREM) sleep facilitates seizure, while the desynchronized EEG of rapid eye movement (REM) sleep suppresses it. We also elucidated that unilateral deep brain stimulation (DBS) of the anterior nucleus of thalamus (ANT) suppresses seizure recurrence. In the present study, we intraperitoneally injected pentylenetetrazol (PTZ, 40 mg/kg) for 14 consecutive days (PTZ kindling) to induce spontaneous seizure in rats, and a 30-min (delivered 10 min before each PTZ injection) or a 3-h DBS of unilateral ANT (delivered 1 h before each PTZ injection) was applied to suppress seizure. The frequency of DBS stimulation was 200 Hz and the electrical current consisted of biphasic square pulses with 50-?A intensity, 100-?s pulse width, and 4.1-ms stimulation interval. Our results found that PTZ-induced spontaneous seizure did not cause a significant change in the quantity of NREM sleep but suppressed the amount of REM sleep. Unilateral ANT DBS prolonged the onset latency of ictal seizure, decreased the spontaneous seizure duration, and increased the survival rate but did not change the amplitude of epileptiform EEGs during ictal period. Unilateral ANT DBS did not significantly alter NREM sleep but increased the amount of REM sleep. An analysis of the spectrograms of fast Fourier transform indicated that the intensities of all frequencies were enhanced during the PTZ-induced ictal period and the subsequent spontaneous seizure. Thirty minutes of unilateral ANT DBS suppressed the augmentation of low-frequency (<10 Hz) intensities during the spontaneous seizure induced by PTZ kindling. We further found that consecutive injections of PTZ progressively increased the enhancement of the delta powers during NREM sleep, whereas unilateral ANT DBS inhibited this progressive enhancement. It was also noticed that 30 min of ANT DBS exhibited a better efficacy in epilepsy suppression than 3 h of ANT DBS. These results elucidated that unilateral ANT DBS enhanced the seizure threshold by increasing the amount of REM sleep and decreasing the progressive enhancement of delta power during NREM sleep to suppress spontaneous seizure recurrences in PTZ kindling-induced epileptic rats.

Project description:Studies ascribe different functions to rapid eye movement (REM) and non-rapid eye movement (NREM) sleep, such that their disruption could result in discrepant clinical outcomes. Although sleep architecture is globally preserved in children with obstructive sleep apnoea (OSA), it is considered to be an REM sleep REMS disorder. Furthermore, body position during sleep affects the occurrence of respiratory events, while the presence of obesity has been claimed to affect sleep-state distribution of respiratory disturbance.To explore the distribution of respiratory events during REMS and NREM sleep NREMS and its potential predictors, a cross-sectional analysis of 335 overnight sleep studies in snoring children from the community was conducted. The ratio of REMS to NREMS respiratory events was compared, and potential associations were assessed using general linear modelling (GLM).Children were 7.3±1.2 years old and had a body mass index (BMI) z-score of 1.0±1.3. The obstructive apnoea-hypopnea index (OAHI) was 1.7±3 and 45.8% of children had an apnoea-hypopnea index (AHI) >1h(-1) total sleep time (TST). Obstructive respiratory events were 3.8 times more likely in REMS (2.0 h(-1)) than NREMS (0.5h(-1)), and the GLM revealed distinctive predictive associations for the apnoeic and hypopneic indices separately, and for body position, the latter indicating that the REMS/NREMS distribution of respiratory events depends on body position.Obstructive respiratory events are predominantly, albeit not exclusively, present in REMS in school-aged children. NREMS respiratory events are more likely in the presence of lower oxyhaemoglobin saturations during event, side body position and in African-American children. However, REMS dominance is not affected by either BMI z-score or obesity. Our findings suggest that incorporating comprehensive respiratory event profiles of children may enhance our understanding of the pathophysiology and adverse outcomes in the context of paediatric OSA.

Dataset Information

Loss of Gnas imprinting differentially affects REM/NREM sleep and cognition in mice.

Publications

Loss of Gnas imprinting differentially affects REM/NREM sleep and cognition in mice.

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