Neural consequences of chronic sleep disruption

Trends in Neurosciences, Год журнала: 2022, Номер 45(9), С. 678 - 691

Опубликована: Июнь 9, 2022

Recent evidence in humans reveals that chronic sleep disruption can lead to protracted recovery of neurobehavioral performance, particularly sustained vigilance and episodic memory.Studies animal models demonstrate even incomplete recovery, including neuron loss brain areas critical for memory, specifically, the locus coeruleus hippocampus.The severity neural injury incurred by varies with duration type disruption, age at which exposure occurs, neuronal populations being assessed, genetic predisposition neurodegenerative processes.Early oxidative stress inflammation contribute a metabolic resetting, behavioral impairment, pathologic findings associated disruption. studies both call into question completeness after Studies have identified cognitive domains vulnerable delayed or memory. These findings, turn, provide focus model critically test lasting impact on brain. Here, we summarize human response then discuss recent examining responses circuits pertinent We propose pathways common various forms consider implications this aging disorders. Chronic humans: evolving thoughts recoveryChronic curtailment is modern society related part increased work demands, lifestyle choices, development use medications substances suppress disrupt sleep, addition artificial light-emitting devices delay sleep. A generally held presumption has been while results impairments, performance deficits are reversed limited-period (e.g., over weekend). collection loss, however, challenges belief suggests impairments persist, additionally, individuals may be poor judges their time. From 1 2 weeks restriction <7 h sleep/night adults shown repeatedly result cumulative increases propensity, along decrements mood [1.Dinges D.F. et al.Cumulative sleepiness, disturbance, psychomotor during week restricted 4-5 hours per night.Sleep. 1997; 20: 267-277PubMed Google Scholar, 2.Van Dongen H.P. al.The cost additional wakefulness: dose-response effects functions physiology from total deprivation.Sleep. 2003; 26: 117-126Crossref PubMed Scopus (2126) 3.Belenky G. al.Patterns degradation restoration subsequent recovery: study.J. Sleep Res. 12: 1-12Crossref (979) Scholar]. Objective subjective discrepancies, were evident, as study participants unaware progressive deterioration across Scholar,2.Van While (sleepiness mood) typically normalized 1–2 nights objective measures showed persistent deficits, relative baseline 2–3 [3.Belenky 4.Banks S. al.Neurobehavioral dynamics following restriction: one night recovery.Sleep. 2010; 33: 1013-1026Crossref 5.Pejovic al.Effects mild interleukin-6 cortisol secretion daytime sleepiness performance.Am. J. Physiol. Endocrinol. Metab. 2013; 305: E890-E896Crossref (105) similarly was evident adolescents [6.Lo J.C. successive cycles without naps adolescents.Sleep. 2017; 40zsw042Crossref (51) In young adults, impaired 5 days 4 h/night restriction, frequency lapses not despite 3 [7.Axelsson al.Sleepiness repeated semi-laboratory conditions.Chronobiol. Int. 2008; 25: 297-308Crossref (93) More recently, field conducted time reduced third 10 consecutive [8.Ochab J.K. al.Observing changes functioning induced deficiency periods.PLoS One. 2021; 16e0255771Crossref (0) Neither accuracy interference assay (Stroop) nor eyes-open alpha power spectra had 7-day period When deprived all 40 hours, resolved tasks requiring higher function reading comprehension, serial addition, go-no-go tasks) did normalize [9.Ikegami K. al.Recovery fatigue deprivation.J. Occup. Health. 2009; 51: 412-422Crossref (28) As deprivation overestimate own [10.Boardman J.M. ability self-monitor 60 sleep.J. 2018; 27e12633Crossref (12) vigilance, impairs memory hippocampal connectivity prefrontal cortex default mode network [11.Chai Y. al.Two restores but deprivation.Sci. Rep. 2020; 10: 8774Crossref (14) connectivity, persists. Collectively, these lines strongly support notion manifest imperceptions impairments. The latter finding contributed false sense security upon weekend sleep.Neurobehavioral largely attributed homeostatic wake-induced extracellular adenosine; levels readily reverse short-term [12.Porkka-Heiskanen T. al.Adenosine: mediator sleep-inducing prolonged wakefulness.Science. 276: 1265-1268Crossref (895) 13.Kalinchuk A.V. course adenosine, nitric oxide (NO) inducible NO synthase role non-rapid eye movement cascade.J. Neurochem. 2011; 116: 260-272Crossref 14.McKenna J.T. al.Sleep fragmentation elevates behavioral, electrographic neurochemical sleepiness.Neuroscience. 2007; 146: 1462-1473Crossref (90) 15.Porkka-Heiskanen al.Brain site-specificity adenosine concentration spontaneous sleep: an vivo microdialysis study.Neuroscience. 2000; 99: 507-517Crossref (376) 16.Portas C.M. al.Role state modulation: freely moving cat.Neuroscience. 79: 225-235Crossref With longer durations do necessarily parallel undergoing deprivation, increase any regions measurements made, hippocampus [17.Zeitzer al.Extracellular deprivation: study.Sleep. 2006; 29: 455-461Crossref (33) study, histories epilepsy, values compared samples allowed determine expected drift rats exposed measured slices reduced, rather than elevated, 2-week opportunity, slice remained below [18.Clasadonte al.Chronic disrupts homeostasis sensitivity alcohol reducing accumulation adenosine.J. Neurosci. 2014; 34: 1879-1891Crossref By contrast, Thus, caused acute loss. However, presence recoveries partial absence elevations raises possibility sleep-loss-induced injury.Neural difficult assess predefined indices indicative glial modification, and/or dysfunction. This challenge illustrated series experiments performed three decades ago, aimed potential cell damage using methodologies available Adult extreme form weeks. resulted profound systemic (severe weight malnutrition, bacterial sepsis, hormonal dysregulation, ultimately death), yet examination brains immediately general histology, apoptosis, necrosis, yielded no significant abnormalities [19.Cirelli C. al.No degeneration long-term rats.Brain 1999; 840: 184-193Crossref Does mean does injure brain? would argue when defined impairment circuit dysfunction, analyses needed exclude injury.With improved definitions, assays strategies paradigm shift emerging, transition considering reversible response, greater appreciation Review, begin highlighting models, emphasizing more how reversibility influenced, only chronicity also exposure, interval used assessment, subtypes regions, propensity protein aggregation. review what learned regarding mechanisms suggest future directions identify therapies lessen commonly encountered scenarios disruption.Neural modelsConsideration paradigmsVarious modalities developed rapid (REM) fragmentation. There some inherent overlap modes For example, definition, includes REM methods impart non-REM (NREM) [20.Arthaud al.Paradoxical mice small-platforms-over-water method: polysomnographic melanin-concentrating hormone hypocretin/orexin activation before, 2015; 24: 309-319Crossref Scholar,21.Silva R.H. mice.Neuropharmacology. 2004; 46: 895-903Crossref (250) simple technique platform-over-water prevent depending size platforms animals studied. platform should adjusted so initiate disrupted, state-dependent reductions postural muscle tone falling water abruptly waking up. Larger control environment; show [22.Machado R.B. modified multiple technique: quantification recovery.Brain 1004: 45-51Crossref (285) Platform approaches elevated plasma corticosterone Scholar,23.Tobler I. effect rat.Neurosci. Lett. 1983; 35: 297-300Crossref Scholar,24.Suchecki D. al.Increased ACTH different paradoxical 1998; 7: 276-281Crossref Additionally, each continuum NREM patterns 24-h cycle.Most date, those discussed here, implemented physical means although it now possible elicit chemogenetic wake [25.Holth sleep-wake cycle regulates interstitial fluid tau CSF humans.Science. 2019; 363: 880-884Crossref (252) Scholar] or, potentially, inactivation circuits. Commonly paradigms types targeted Figure 1, advantages, disadvantages, confounding factors. there differences level arousal amount learning experienced where exploratory wakefulness induce robust immediate early gene wake-activated neurons, gentle handling same [26.Deurveilher al.Social environmental contexts modulate deprivation-induced c-Fos rats.Behav. Brain 256: 238-249Crossref (8) Exploratory locomotor activity, providing continuously enriched changing environment, involve other constant (or expected) environments. Techniques require continuous experimenter like handling, allow breakthrough automated systems rotating platform) intervene soon electroencephalographic detected computer algorithm [27.Leenaars C.H. al.A new method rat minimal activity.J. Methods. 196: 107-117Crossref Scholar,28.Deboer al.Long term mammalian circadian pacemaker.Sleep. 30: 257-262Crossref elicited either bar sweeping floor cage set intervals way rotor table briskly moves cages fraction every minute two. Methods fragment shorten amounts [29.Sinton al.Validation novel interrupt mouse.J. 184: 71-78Crossref approach effective long periods (weeks) seems influence body [30.Li wake-active neurons hypercapnic response.Sleep. 37: 51-64Crossref Scholar,31.Wallace E. al.Differential spatial synaptic plasticity pubertal mice.Brain 1615: 116-128Crossref (15) allows group housing, ad libitum eating drinking, access undisturbed nests. sweeper nests cannot maintained, group-housed. its strengths limitations, techniques provided similar results.Locus coeruleus: hitDelayed supports concept could affect within circuit, anterior cingulate cortical [32.Gompf H.S. al.Locus ceruleus sustain environment.J. 14543-14551Crossref (109) Locus (LCn) noradrenergic pontine firing rates highest unexpected uncertainties Scholar,33.Bliss-Moreau al.Anterior ablation affective vigor vigilance.J. 41: 8075-8087Crossref (4) change wakefulness, influences LCn. Upon brief (3 h) LCn adult upregulate mitochondrial deacetylase sirtuin (SirT3), initiates antioxidant maintain redox [34.Zhang al.Extended compromised metabolics neurons.J. 4418-4431Crossref (Figure 2) . 8 wakefulness/day environment paradigm, SirT3 activating enzymes upregulated develop stress, acetylation, acetylation electron transport chain proteins, counts Whether observed represent adaptation dysfunction injury, requires point further termination outlined above adaptive temporarily downregulate activity tyrosine hydroxylase; marker forementioned study. Of note, noradrenaline metabolites, 3,4-dihydroxyphenylglycoaldehyde, modifies tau, increasing aggregate propagate [35.Kang S.S. al.Norepinephrine metabolite DOPEGAL activates AEP pathological Tau aggregation coeruleus.J. Clin. Invest. 130: 422-437Crossref (26) hydroxylase faced restriction. According scenario, once reinstated, resume. continued 12 weeks, year counts, [36.Owen J.E. al.Late-in-life neurodegeneration mice.Sleep. 44zsab057Crossref (7) Scholar], indicating irreversible Similarly, whole-cell patch clamp recordings step currents after-hyperpolarization amplitudes supporting functional [37.Li hypercapneic remaining LCn, [38.Zhu al.Degeneration modeling apnea.Front. Neurol. 6: 109Crossref Not studies, One rats, instance, drum alternated enforced ambulation rest, days/week nonrotating drums [39.Deurveilher orexin/hypocretin, restriction.Eur. 54: 6027-6043Crossref count variability high controls, conceivable brevity prevented engaged protective wakefulness. output Rats task, [40.Lu H.J. Lv β-Adrenergic receptor dentate gyrus participates sleep-deprived rats.Exp. Neurobiol. 144-154Crossref Because unclear whether reduction represents dysfunction.Figure 2Duration-dependent (LCn).Show full captionShort-term [awake habitual (lights-on) period] upregulates (SirT3) nuclear translocation FoxO3a transcriptional antioxidants PGC-1α enhance biogenesis. extended (for day lights-on days) reduces NAD+-synthesizing enzymes, thereby (and inactivating) FoxO3a. Mechanisms switch maladaptive known.View Large Image ViewerDownload Hi-res image Download (PPT)Why disruption? status dictate vulnerability Mice deficient lower baseline, decline suggesting susceptible waking. second because exposures [41.Vankov A. al.Response novelty habituation exploring rat.Eur. 1995; 1180-1187Crossref (201) most active autoreceptor lowest, [42.Aston-Jones Bloom F.E. Activity norepinephrine-containing behaving anticipates fluctuations sleep-waking cycle.J. 1981; 1: 876-886Crossref Opening l-type calcium channels arousal, mitochondria activate calcium-dependent synthesis, impairing superoxide production [43.Sanchez-Padilla al.Mitochondrial oxidant regulated synthase.Nat. 17: 832-840Crossref (92) identification underlying (see Outstanding questions), determined implemented, resolve perturbance.Hippocampal disruptionIn humans, hippocampal-dependent persist Th

Язык: Английский

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Sleep deprivation: A risk factor for the pathogenesis and progression of Alzheimer's disease

Heliyon, Год журнала: 2024, Номер 10(7), С. e28819 - e28819

Опубликована: Апрель 1, 2024

Sleep deprivation refers to an intentional or unintentional reduction in sleep time, resulting insufficient sleep. It is often caused by disorders, work demands (e.g., night shifts), and study pressure. promotes Aβ deposition tau hyperphosphorylation, which a risk factor for the pathogenesis progression of Alzheimer's disease (AD). Recent research has demonstrated potential involvement both AD through glial cell activation, lymphatic system, orexin circadian rhythm inflammation, gut microbiota. Thus, investigating molecular mechanisms underlying association between crucial, may contribute development preventive therapeutic strategies AD. This review aims analyze impact on AD, exploring pathological that link initiation offers theoretical foundation drugs aimed at preventing treating

Язык: Английский

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Crocin (bioactive compound of Crocus sativus L.) potently restores REM sleep deprivation-induced manic- and obsessive-compulsive-like behaviors in female rats

Behavioural Pharmacology, Год журнала: 2024, Номер unknown

Опубликована: Март 29, 2024

Rapid-eye movement (REM) sleep deprivation (SD) can induce manic-like behaviors including hyperlocomotion. On the other hand, crocin (one of main compounds Crocus sativus L. or Saffron) may be beneficial in improvement mental and cognitive dysfunctions. Also, restore deleterious effects SD on processes. In this study, we investigated effect REM female rats’ depression- anxiety-like behaviors, locomotion, pain perception, obsessive-compulsive-like behavior, also, potential effects. We used rats because evidence role modulating psychological behavioral functions (but not male) is limited. was induced for 14 days (6h/day), (25, 50, 75 mg/kg) injected intraperitoneally. Open field test, forced swim hot plate marble burying test were to assess behaviors. The results showed SD-induced behavior (hyperlocomotion). decreased anxiety- depression-like subthreshold (the duration it takes rat feel pain), obsessive compulsive-like behavior. However, at all doses partially fully reversed changes. conclusion, our suggested possible comorbidity OCD etiology OCD, although more studies are needed. contrast, a therapeutic choice decreasing

Язык: Английский

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The interaction between orexin, sleep deprivation and Alzheimer’s disease: Unveiling an Emerging Connection

The Journal of Physiological Sciences, Год журнала: 2025, Номер 75(1), С. 100004 - 100004

Опубликована: Март 1, 2025

Язык: Английский

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Understanding neuron-glia crosstalk and biological clocks in insomnia

Neuroscience & Biobehavioral Reviews, Год журнала: 2023, Номер 147, С. 105100 - 105100

Опубликована: Фев. 17, 2023

According to the World Health Organization, about one-third of population experiences insomnia symptoms, and 10-15% suffer from chronic insomnia, most common sleep disorder. Sleeping difficulties associated with are often linked deprivation, which has a negative health impact partly due disruption in internal synchronisation biological clocks. These regulated by clock genes modulate processes. Most studies addressing circadian rhythm regulation have focused on role neurons, yet glial cells also rhythms regulation. Chronic loss been cell activation, exacerbated neuroinflammation, oxidative stress, altered neuronal metabolism synaptic plasticity, accelerated age-related processes decreased lifespan. It is, therefore, essential highlight importance glia-neuron interplay sleep/circadian overall healthy brain function. Hence, this review, we aim address main neurobiological mechanisms involved neuron-glia crosstalk, an emphasis microglia astrocytes, both sleep, deprivation insomnia.

Язык: Английский

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Sleep deficiency promotes Alzheimer's disease development and progression

Frontiers in Neurology, Год журнала: 2022, Номер 13

Опубликована: Дек. 14, 2022

Sleep disorders are a common health problem in modern society. Long-term sleep deficiency increases the risk for Alzheimer's disease. However, exact mechanisms by which affects disease remain unclear. Therefore, we reviewed relevant studies and investigated role of deprivation pathogenesis. was found to be associated with oxidative stress, β-amyloid protein deposition, tau hyperphosphorylation, neuroinflammation, known increase In addition, insufficient also glucocorticoid levels, decreases brain-derived neurotrophic factor reduces number synapses central nervous system. These factors promote development progression. The present study showed that growing body evidence supports an association between disturbances It discusses insufficiency pathogenesis, may provide theoretical basis effective treatment prevention strategies.

Язык: Английский

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Immunotherapy in Alzheimer’s Disease: Current Status and Future Directions

Journal of Alzheimer s Disease, Год журнала: 2024, Номер 101(s1), С. S23 - S39

Опубликована: Окт. 18, 2024

Alzheimer's disease (AD) is a progressive neurological disorder characterized by memory loss, cognitive decline, and behavioral changes. Immunotherapy aims to harness the immune system target underlying pathology of AD has shown promise as disease-modifying treatment for AD. By focusing on pathogenesis encouraging removal abnormal protein aggregates in brain, immunotherapy shows potential The development began with early attempts use antibodies beta-amyloid. amyloid hypothesis which suggests that accumulation beta-amyloid brain triggers pathological cascade leads been driving force behind However, recent clinical trials monoclonal targeting amyloid-β have mixed results, highlighting need further research into alternative approaches. Additionally, safety efficacy remain an area active investigation. Some immunotherapeutic approaches promise, while others associated significant side effects, including inflammation brain. Sleep impact various physiological processes, system, linked Thus, improving sleep quality duration may benefit potentially enhance effectiveness In this review, we discussed promises well possible methods improve achieve better therapeutic outcomes.

Язык: Английский

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Ptprd deficiency promotes tau hyperphosphorylation and impairs cognitive function in aged mice

Biological Research, Год журнала: 2025, Номер 58(1)

Опубликована: Май 6, 2025

Язык: Английский

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Orexin-A aggravates cognitive deficits in 3xTg-AD mice by exacerbating synaptic plasticity impairment and affecting amyloid β metabolism

Neurobiology of Aging, Год журнала: 2023, Номер 124, С. 71 - 84

Опубликована: Янв. 18, 2023

Язык: Английский

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REM sleep deprivation induced by the modified multi-platform method has detrimental effects on memory: A systematic review and meta-analysis

Behavioural Brain Research, Год журнала: 2023, Номер 454, С. 114652 - 114652

Опубликована: Авг. 30, 2023

The modified multi-platform method (MMPM) is used to induce animal models of paradoxical sleep deprivation and impairs memory in rodents. However, variations MMPM protocols have contributed inconsistent conclusions across studies. This meta-analysis aimed assess the their effects on rats mice. A comprehensive search identified 60 studies, 50 were included our meta-analysis. Overall, showed that significantly reduced percentage time spent target quadrants (I2 = 54 %, 95 % confidence interval [CI] [-1.83, -1.18]) number platform-area crossings 26 CI [-1.71, -1.07]) Morris water maze (MWM) shortened latency entering dark compartment passive avoidance task 68 [-1.36, -0.57]), but it increased errors radial arm (RAWM) 59 [1.29, 2.07]). Additionally, mice performed worse MWM, whereas task. More significant deficits found cross-learning post-learning MWM RAWM, respectively. study provided evidence can be preclinical studies induced by deprivation.

Язык: Английский

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