The stress of losing sleep: Sex-specific neurobiological outcomes

Wright, Courtney J.; Milosavljevic, Snezana; Pocivavsek, Ana

doi:10.1016/j.ynstr.2023.100543

Cited by 18 publications

(4 citation statements)

References 555 publications

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“…Multiple sleep deprivation protocols were used, such as MSP (multiple small platforms), CP (classical platform/inverted flowerpot), DOW (Disk over water), GH (Gentle handling) and ASD (automated sleep deprivation). Comprehensive descriptions of the mentioned sleep deprivation protocols and respective control groups have been previously reviewed [ 9 , 24 , 25 ].…”

Section: Resultsmentioning

confidence: 99%

“…Based on the currently limited evidence from animal and human studies, it appears that sleep loss may have a potentially greater impact on cognition in females compared to males [ 81 ]. Additionally, some data seem to suggest that females may exhibit a greater stress response to sleep disturbances (HPA reactivity, sympathetic nervous system activation, cardiovascular dysfunction), increased mood disruptions and possibly even an increased inflammatory response [ 25 ]. As previously reviewed [ 82 ], sex differences between male and female rodents seem to influence multiple characteristics of sleep, such as duration, time spent in different sleep phases, sleep fragmentation, circadian functions and the response to SD.…”

Section: Discussionmentioning

confidence: 99%

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Sleep Deprivation-Induced Oxidative Stress in Rat Models: A Scoping Systematic Review

et al. 2023

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Sleep deprivation is highly prevalent in the modern world, possibly reaching epidemic proportions. While multiple theories regarding the roles of sleep exist (inactivity, energy conservation, restoration, brain plasticity and antioxidant), multiple unknowns still remain regarding the proposed antioxidant roles of sleep. The existing experimental evidence is often contradicting, with studies pointing both toward and against the presence of oxidative stress after sleep deprivation. The main goals of this review were to analyze the existing experimental data regarding the relationship between sleep deprivation and oxidative stress, to attempt to further clarify multiple aspects surrounding this relationship and to identify current knowledge gaps. Systematic searches were conducted in three major online databases for experimental studies performed on rat models with oxidative stress measurements, published between 2015 and 2022. A total of 54 studies were included in the review. Most results seem to point to changes in oxidative stress parameters after sleep deprivation, further suggesting an antioxidant role of sleep. Alterations in these parameters were observed in both paradoxical and total sleep deprivation protocols and in multiple rat strains. Furthermore, the effects of sleep deprivation seem to extend beyond the central nervous system, affecting multiple other body sites in the periphery. Sleep recovery seems to be characterized by an increased variability, with the presence of both normalizations in some parameters and long-lasting changes after sleep deprivation. Surprisingly, most studies revealed the presence of a stress response following sleep deprivation. However, the origin and the impact of the stress response during sleep deprivation remain somewhat unclear. While a definitive exclusion of the influence of the sleep deprivation protocol on the stress response is not possible, the available data seem to suggest that the observed stress response may be determined by sleep deprivation itself as opposed to the experimental conditions. Due to this fact, the observed oxidative changes could be attributed directly to sleep deprivation.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Sleep Deprivation-Induced Oxidative Stress in Rat Models: A Scoping Systematic Review

et al. 2023

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“…We used only male mice instead of a sex‐mixed population. Sex differences in the responses to sleep deprivation interventions have been noted (Krishnan & Collop, 2006; Wright et al., 2023). It is equally important to study sleep fragmentation in female mice, so this is a main limitation of this study.…”

Section: Limitationmentioning

confidence: 99%

Sleep fragmentation reduces explorative behaviors and impairs motor coordination in male mice

Xiong,

Zhu,

et al. 2023

J of Neuroscience Research

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Sleep fragmentation (SF), which refers to discontinuous and fragmented sleep, induces cognitive impairment and anxiety‐like behavior in mice. However, whether SF can affect motor capability in healthy young wild‐type mice and the underlying mechanisms remain unknown. We performed seven days of sleep fragmentation (SF 7d) interventions in young wild‐type male mice. While SF mice experienced regular sleep disruption between Zeitgeber time (ZT) 0–12, control mice were allowed to have natural sleep (NS) cycles. Homecage analysis and conventional behavioral tests were conducted to assess the behavioral alterations in behavioral patterns in general and motor‐related behaviors. Sleep structures and the power spectrum of electroencephalograms (EEGs) were compared between SF 7d and NS groups. Neuronal activation was measured using c‐Fos immunostaining and quantified in multiple brain regions. SF of 7 days significantly decreased bouts of rearing and sniffing and the duration of rearing and impaired motor coordination. An increase in the total sleep time and a decrease in wakefulness between ZT12–24 was found in SF 7d mice. In SF 7d mice, EEG beta1 power was increased in rapid eye movement (REM) sleep while theta power was decreased during wakefulness. SF 7d resulted in significant suppression in c‐Fos (+) cell counts in the motor cortex and hippocampus but an increase in c‐Fos (+) cell counts in the substantia nigra pars compacta (SNc). In summary, SF 7d suppressed explorative behaviors and impaired motor coordination as compared to NS. EEG power and altered neuronal activity detected by c‐Fos staining might contribute to the behavioral changes.

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“…Biological sex is also a critically important factor in understanding the role of sleep disruption in the progression of AD and Tau pathology. Males and females have been shown to have differential likelihoods of developing neurodegenerative conditions ( Sinforiani et al, 2010 ) and also have been found to respond differentially to sleep deprivation (SD; Wright et al, 2023 ), suggesting that there may be sex-specific vulnerabilities to the negative consequences of sleep loss.…”

Section: Introductionmentioning

confidence: 99%

Sleep Disruption Precedes Forebrain Synaptic Tau Burden and Contributes to Cognitive Decline in a Sex-Dependent Manner in the P301S Tau Transgenic Mouse Model

Martin,

Joyce,

Lord

et al. 2024

eNeuro

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Sleep disruption and impaired synaptic processes are common features in neurodegenerative diseases, including Alzheimer's disease (AD). Hyperphosphorylated Tau is known to accumulate at neuronal synapses in AD, contributing to synapse dysfunction. However, it remains unclear how sleep disruption and synapse pathology interact to contribute to cognitive decline. Here, we examined sex-specific onset and consequences of sleep loss in AD/tauopathy model PS19 mice. Using a piezoelectric home-cage monitoring system, we showed PS19 mice exhibited early-onset and progressive hyperarousal, a selective dark-phase sleep disruption, apparent at 3 months in females and 6 months in males. Using the Morris water maze test, we report that chronic sleep disruption (CSD) accelerated the onset of decline of hippocampal spatial memory in PS19 males only. Hyperarousal occurs well in advance of robust forebrain synaptic Tau burden that becomes apparent at 6–9 months. To determine whether a causal link exists between sleep disruption and synaptic Tau hyperphosphorylation, we examined the correlation between sleep behavior and synaptic Tau, or exposed mice to acute or chronic sleep disruption at 6 months. While we confirm that sleep disruption is a driver of Tau hyperphosphorylation in neurons of the locus ceruleus, we were unable to show any causal link between sleep loss and Tau burden in forebrain synapses. Despite the finding that hyperarousal appears earlier in females, female cognition was resilient to the effects of sleep disruption. We conclude sleep disruption interacts with the synaptic Tau burden to accelerate the onset of cognitive decline with greater vulnerability in males.

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The stress of losing sleep: Sex-specific neurobiological outcomes

Cited by 18 publications

References 555 publications

Sleep Deprivation-Induced Oxidative Stress in Rat Models: A Scoping Systematic Review

Sleep Deprivation-Induced Oxidative Stress in Rat Models: A Scoping Systematic Review

Sleep fragmentation reduces explorative behaviors and impairs motor coordination in male mice

Sleep Disruption Precedes Forebrain Synaptic Tau Burden and Contributes to Cognitive Decline in a Sex-Dependent Manner in the P301S Tau Transgenic Mouse Model

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