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Chronic sleep fragmentation impairs brain interstitial clearance in young wildtype mice
Open accessAbstract
Accumulating evidence shows that most chronic neurological diseases have a link with sleep disturbances, and that patients with chronically poor sleep undergo an accelerated cognitive decline. Indeed, a single-night of sleep deprivation may increase metabolic waste levels in cerebrospinal fluid. However, it remains unknown how chronic sleep disturbances in isolation from an underlying neurological disease may affect the glymphatic system. Clearance of brain interstitial waste by the glymphatic system occurs primarily during sleep, driven by multiple oscillators including arterial pulsatility, and vasomotion. Herein, we induced sleep fragmentation in young wildtype mice and assessed the effects on glymphatic activity and cognitive functions. Chronic sleep fragmentation reduced glymphatic function and impaired cognitive functions in healthy mice. A mechanistic analysis showed that the chronic sleep fragmentation suppressed slow vasomotion, without altering cardiac-driven pulsations. Taken together, results of this study document that chronic sleep fragmentation suppresses brain metabolite clearance and impairs cognition, even in the absence of disease.
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Written from the paper’s full text.
TL;DR
In young healthy wildtype mice, 30 days of chronic sleep fragmentation impaired glymphatic CSF tracer influx/efflux and exogenous Aβ1-40 clearance and impaired cognition, whereas 3 days did not. The effect was associated with suppressed slow vasomotion, not altered cardiac-driven pulsatility.
Key findings
- Chronic sleep fragmentation for 30 days reduced glymphatic function: CSF tracer intensity and area fraction were significantly lower in cortex and subcortex but not hippocampus, tracer efflux to deep cervical lymph nodes was suppressed, and clearance of exogenous human Aβ1-40 from prefrontal cortex was significantly decreased (N = 5 per group).
- Acute sleep fragmentation for 3 days did not alter glymphatic tracer influx, dCLN tracer efflux, or Aβ1-40 clearance; Aβ clearance showed a non-significant trend toward increase.
- SF 30 days suppressed slow vasomotion: power spectral density in the low frequency band 0.05–0.15 Hz was significantly lower, and amplitude at 0.1 Hz was significantly reduced (n = 23 arteries from five SF 30 days mice vs n = 20 arteries from four controls), while cardiac-driven pulsatility was unchanged. SF 3 days did not alter slow vasomotion or cardiac pulsatility.
- Both SF 3 days and SF 30 days impaired novel object recognition and increased anxiety-like behavior in the open field; SF 30 days also increased EEG theta prevalence during ZT 5–12 (N = 5 vs 6), with no significant change in blood-brain barrier permeability.
Methods
- Male C57BL/6 wildtype mice aged 2–3 months and weighing 25–30 g were exposed to sleep fragmentation by orbital rotor shaking at 110 rpm for 10 sec every 2 min during the light phase for 3 or 30 consecutive days; controls were undisturbed.
- Glymphatic function was assessed by cisterna magna infusion of 40 kDa FITC-dextran with quantification of tracer intensity/area in brain regions and deep cervical lymph nodes, plus ELISA measurement of exogenous human Aβ1-40 clearance from prefrontal cortex.
- In vivo two-photon imaging through a chronic cranial window measured cardiac-driven vascular pulsatility and slow vasomotion; EEG/EMG, open field, novel object recognition, immunofluorescence for AQP4/CD31/LYVE1, and GraphPad Prism statistics (t tests, Mann-Whitney, two-way ANOVA) were also used.
Limitations
- Stated: “Our exclusive use of male mice limits the generalizability of present results.”
- Stated: it remains to be determined whether respiration contributes to sleep-fragmentation-induced glymphatic suppression, and whether cerebral blood volume/CSF phenomena overlap.
- Evident from the text: the study is restricted to young male wildtype mice, so effects in females, aged animals, or disease models are not tested; the proposed norepinephrine/HPA mechanism is discussed but not directly manipulated.
Model-written summary. Check it against the paper before relying on it.
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Claims the paper makes
0 of 65 cited sources checked · 0 supported · 0 flagged
- Findingown data
The area fraction of the LYVE1 positive region in SF 30 days mice showed a trend towards reduction as compared with controls.
“The area fraction of the LYVE1 positive region in SF 3 days mice was comparable with controls (Figure 2j-k), while the area fraction in SF 30 days mice showed a trend towards reduction as compared with controls (Figure 3j-k).”
Quote in the paperNot a substantial claim - Findingown data
There was a slight but significant reduction in the declining slope of AQP4 fluorescence signal as a function of distance from the vessel wall in SF 30 days mice versus controls.
“We found a slight but significant reduction in the declining slope in SF 30 days mice versus controls, suggesting that AQP4 protein expression was less polarized around the vascular wall after 30 days of SF (Figure 5a-c).”
Quote in the paperSubstantial claim - Findingown data
Slow vasomotion did not differ between SF 3 days and controls across all frequency bands.
“Slow vasomotion did not differ between SF 3 days and controls across all frequency bands (Figure 4e, g).”
Quote in the paperNot a substantial claim - Findingown data
Sleep fragmentation groups showed reduced entering of the central zone.
“Sleep fragmentation groups showed reduced entering of the central zone, suggesting anxiety-like behavior (Figure 1f).”
Quote in the paperSubstantial claim - Findingown data
Perivascular fluorescence tracer distribution around cortical penetrating vessels was suppressed by SF 30 days.
“The perivascular fluorescence tracer distribution around the cortical penetrating vessels was suppressed by SF 30 days (Figure 3b, zoom-in view).”
Quote in the paperSubstantial claim
- Findingown data
The area fraction of the LYVE1 positive region in SF 3 days mice was comparable with controls.
“The area fraction of the LYVE1 positive region in SF 3 days mice was comparable with controls (Figure 2j-k), while the area fraction in SF 30 days mice showed a trend towards reduction as compared with controls (Figure 3j-k).”
Quote in the paperNot a substantial claim - Findingown data
Delta prevalence and other power bands did not differ significantly between SF 30 days and controls.
“Delta prevalence and other power bands did not differ significantly (Figure 5f-g).”
Quote in the paperSubstantial claim - Findingown data
Theta prevalence was significantly higher in SF 30 days mice than in normal sleep controls.
“Present results for the EEG power spectrum density recorded at ZT 5-12 showed that theta prevalence was significantly higher in SF 30 days mice than in normal sleep controls.”
Quote in the paperNot a substantial claim - Findingown data
Chronic sleep fragmentation impairs cognitive functions in healthy mice.
“Chronic sleep fragmentation reduced glymphatic function and impaired cognitive functions in healthy mice.”
Quote in the paperSubstantial claim - Findingown data
Macroscopic imaging of whole brains showed that CSF tracer fluorescence was lower in SF 30 days mice versus normal sleep controls.
“Macroscopic imaging of whole brains showed that the CSF tracer fluorescence was lower in SF 30 days mice versus normal sleep controls (Figure 3a).”
Quote in the paperSubstantial claim - Findingown data
In the present study, there was a trend towards attenuation of the vasodynamics in the frequency range 0.15-0.60 Hz in the SF 30 days treatment group.
“In the present study, there was a trend towards attenuation of the vasodynamics in the frequency range 0.15-0.60Hz in the SF 30 days treatment group (Figure 4).”
Quote in the paperNot a substantial claim - Findingown data
SF 3 days or SF 30 days treatments were without effects on cardiac-driven arterial pulsatility.
“In our two-photon microscopy evaluation, SF 3 days or SF 30 days treatments were without effects on cardiac-driven arterial pulsatility.”
Quote in the paperSubstantial claim - Findingown data
Chronic sleep fragmentation reduces glymphatic function in healthy mice.
“Chronic sleep fragmentation reduced glymphatic function and impaired cognitive functions in healthy mice.”
Quote in the paperSubstantial claim - Findingown data
The amplitudes of the frequency spectrum at 0.05 or 0.1 Hz were similar between SF 3 days and controls groups.
“The amplitudes of the frequency spectrum at 0.05 or 0.1 Hz were similar between SF 3 days and controls groups (Figure 4i).”
Quote in the paperNot a substantial claim - Findingown data
The mean intensity of fluorescence and area covered by tracer in neck lymph node did not exhibit significant differences between SF 3 days and control.
“Neither did the mean intensity of fluorescence and area covered by tracer in neck lymph node exhibit significant differences between the two groups (Figures 2e-g).”
Quote in the paperSubstantial claim - Findingown data
There were no statistical differences in tracer signal intensity and area fractions in cortex, subcortex, hippocampus, or whole brain regions between SF 3 days and control.
“There were no statistical differences in tracer signal intensity and area fractions in cortex, subcortex, hippocampus, or the whole brain regions between the SF 3 days group and control group (Figures 2b-d).”
Quote in the paperSubstantial claim - Findingown data
The power spectrum density of frequency bands (0.05-0.15 Hz, low) was significantly lower in mice exposed to SF 30 days compared with controls.
“The power spectrum density of frequency bands (0.05-0.15 Hz, low) was significantly lower in mice exposed to SF 30 days compared with controls (Figure 4f).”
Quote in the paperSubstantial claim - Findingown data
Total AQP4 protein level in brain homogenates was not altered by SF 30 days.
“Total AQP4 protein level in brain homogenates was not altered by SF 30 days (Figure 5d; Supplementary Figure 1).”
Quote in the paperSubstantial claim - Findingown data
Clearance of exogenous human Amyloid-b1-40 infused into the prefrontal cortex revealed a non-significant trend towards increased clearance in the SF 3 days group compared to normal sleep controls.
“An evaluation of clearance of exogenous human Amyloid-b1-40 infused into the prefrontal cortex revealed a non-significant trend towards increased clearance in the SF 3 days group as compared to normal sleep controls (Figure 2h-i).”
Quote in the paperNot a substantial claim - Findingown data
Neither SF 3 days nor SF 30 days treatments altered Evans Blue uptake relative to control mice.
“The analysis showed that neither SF 3 days nor SF 30 days treatments altered Evans Blue uptake relative to control mice, indicating a lack of effect of acute and chronic sleep deprivation on BBB permeability.”
Quote in the paperSubstantial claim - Findingown data
Mean tracer intensity and influx area in brain slices extending from rostral to caudal was significantly lower in SF 30 days mice compared with normal sleep controls.
“An analysis of CSF tracer influx in the coronal brain sections with standard methods, 14,35 revealed that the mean tracer intensity and influx area in brain slices extending from rostral to caudal was significantly lower in SF 30 days mice as compared with normal sleep controls (Figure 3b-d).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [14]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [35]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Findingown data
Assessment of vascular cardiac-driven pulsatility in awake mice did not reveal significant changes in SF 30 days mice as compared with controls.
“Our present assessment of vascular cardiac-driven pulsatility in awake mice through a chronic cranial window did not reveal significant changes in SF 30 days mice as compared with controls (Figure 4a, c).”
Quote in the paperSubstantial claim - Findingown data
The amplitude of the power spectrum density at 0.1 Hz was significantly reduced in SF 30 days mice versus control mice.
“Comparing the amplitude of the power spectrum density at 0.05 and 0.1 Hz showed a significant reduction in amplitude at 0.1 Hz in SF 30 days mice versus control mice (Figure 4h, j).”
Quote in the paperSubstantial claim - Findingown data
Both sleep fragmentation groups showed comparable total distance traveled with their control groups in the open field test.
“The open field test showed that both sleep fragmentation groups showed comparable total distance traveled with their control groups (Figure 1e-g).”
Quote in the paperNot a substantial claim - Findingown data
Clearance of exogenous infused Amyloid b1-40 in prefrontal cortex was significantly decreased in SF 30 days versus normal sleep control mice.
“In addition, the clearance of exogenous infused Amyloid b1-40 in prefrontal cortex was significantly decreased in SF 30 days versus normal sleep control mice (Figure 3h-i).”
Quote in the paperSubstantial claim - Findingown data
There was only a trend towards a reduction in vascular AQP4 in SF 30 days mice.
“We purified cerebral vessels to measure the perivascular AQP4 expression (Figure 5e; Supplementary Figure 1), 42 finding only a trend towards a reduction in vascular AQP4 in SF 30 days mice (Figure 5e).”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [42]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Findingown data
Tracer efflux to the deep cervical lymph nodes was suppressed in SF 30 days mice compared with controls.
“Ex vivo analysis of the lymph nodes showed that tracer efflux to the dCLNs was suppressed in SF 30 days mice compared with controls (Figure 3e-g).”
Quote in the paperSubstantial claim - Findingown data
There was a non-significant trend towards reduced ratio of fluorescence intensity between the perivascular area and neighboring parenchymal regions in SF 30 days mice.
“We saw a non-significant trend towards reduced ratio of fluorescence intensity between the perivascular area and neighboring parenchymal regions in SF 30 days mice (Figure 5c).”
Quote in the paperNot a substantial claim - Findingown data
Acute three days SF does not alter glymphatic function.
“Figure 2 . Figure 2. Acute three days SF does not alter glymphatic function.”
Quote in the paperSubstantial claim - Findingown data
Chronic sleep fragmentation suppresses glymphatic function.
“Figure 3 . Figure 3. Chronic sleep fragmentation suppresses glymphatic function.”
Quote in the paperSubstantial claim - Findingown data
SF 30 days mice showed only minor changes in AQP4 polarization versus control.
“However, we saw only minor changes in AQP4 polarization in SF 30 days mice versus control (Figure 5), rendering it unlikely that AQP4 is involved in SF-induced suppression of glymphatic flow.”
Quote in the paperSubstantial claim - Findingown data
Chronic sleep fragmentation alters the brain vascular function.
“Figure 4 . Figure 4. Chronic sleep fragmentation alters the brain vascular function.”
Quote in the paperNot a substantial claim - Interpretationown data
AQP4 protein expression was less polarized around the vascular wall after 30 days of SF.
“We found a slight but significant reduction in the declining slope in SF 30 days mice versus controls, suggesting that AQP4 protein expression was less polarized around the vascular wall after 30 days of SF (Figure 5a-c).”
Quote in the paperSubstantial claim - Interpretationown data
Brain glymphatic function was unaffected by acute sleep fragmentation lasting three days.
“In summary, brain glymphatic function was unaffected by acute sleep fragmentation lasting three days.”
Quote in the paperSubstantial claim - Interpretationreasoning
The modest changes in AQP4 vascular polarization suggest that reactive changes in astrocytes are not a major factor in the suppression of glymphatic transport observed in SF 30 days mice.
“Thus, the modest changes in AQP4 vascular polarization suggest that reactive changes in astrocytes are not a major factor in the suppression of glymphatic transport observed in SF 30 days mice.”
Quote in the paperSubstantial claim - Interpretationown data
SF did not significantly alter area of meningeal lymph vessels.
“Therefore, SF did not significantly alter area of meningeal lymph vessels.”
Quote in the paperNot a substantial claim - Interpretationown data
Sleep fragmentation of three days does not alter vascular function as regards to cardiac pulsatility or slow vasomotion in awake mice.
“The data suggests that sleep fragmentation of three days does not alter vascular function as regards to cardiac pulsatility or slow vasomotion in awake mice.”
Quote in the paperNot a substantial claim - Premisecitation
SF 30 days treatment significantly suppressed functional hyperemia upon whisker stimulation compared with control animals.
“We recently reported the SF 30 days treatment significantly suppressed the functional hyperemia upon whisker stimulation as compared with control animals.29”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [29]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Premisecitation
The glymphatic system facilitates the export of neurotoxic metabolic wastes that accumulate in brain during wakefulness.
“The glymphatic system, which functionally resembles in many aspects the lymphatic system in peripheral tissues, facilitates the export of neurotoxic metabolic wastes that accumulate in brain during wakefulness.3,14”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [3]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [14]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Interpretationreasoning
Repetitive sleep interruptions perturb cerebrovascular dynamics.
“We thus draw the conclusion that slow vasomotion, but not cardiacdriven arterial pulsatility, is suppressed by chronic sleep fragmentation, which would imply that that repetitive sleep interruptions perturb cerebrovascular dynamics.”
Quote in the paperSubstantial claim - Premisecitation
Glymphatic influx is higher during the light-on phase between ZT 5-12 while mice are primarily inactive compared with the light-off, active phase.
“During the light-on phase between ZT 5-12, while the mice were primarily inactive, glymphatic influx was higher as compared with the light-off, active phase.2”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [2]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Study design and conductcitation
The sleep fragmentation protocol's patency has been established in previous studies.
“We have established the patency of this protocol in our previous studies.13,25”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [13]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [25]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Interpretationown data
The absence of significant vascular functional changes in SF 3 days mice is consistent with the lacking effects on the glymphatic system.
“The absence of significant vascular functional changes in SF 3 days mice seems consistent with the lacking effects on glymphatic system (Figure 2).”
Quote in the paperSubstantial claim - Premisecitation
Chronic sleep fragmentation in healthy young wildtype mice increases intracellular Ab accumulation.
“We previously reported that chronic sleep fragmentation in healthy young wildtype mice increased intracellular Ab accumulation. 13”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [13]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Interpretationown data
This is the first study documenting that chronic sleep fragmentation potently suppresses glymphatic fluid transport in the absence of an underlying neurological disorder.
“To our knowledge, this is the first study documenting that chronic sleep fragmentation potently suppresses glymphatic fluid transport in the absence of an underlying neurological disorder.”
Quote in the paperSubstantial claim - Interpretationreasoning
Vascular function plays an important role in glymphatic function regulation.
“These findings highlight that vascular function plays important role in glymphatic function regulation.”
Quote in the paperSubstantial claim - Interpretationown data
The reduced central zone entering suggests anxiety-like behavior.
“Sleep fragmentation groups showed reduced entering of the central zone, suggesting anxiety-like behavior (Figure 1f).”
Quote in the paperSubstantial claim - Interpretationreasoning
Norepinephrine dysregulation due to chronic sleep fragmentation may contribute to glymphatic impairments.
“Based on these findings, we propose that norepinephrine dysregulation due to chronic sleep fragmentation may contribute to glymphatic impairments.”
Quote in the paperSubstantial claim - Premisecitation
Pharmacological blockade of adrenergic receptors significantly enhances glymphatic influx.
“For example, pharmacological blockade of adrenergic receptors significantly enhances glymphatic influx.3”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [3]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Interpretationnone given
This is the first study to document that sleep fragmentation, in the absence of an underlying neurological or medical disorder, impairs glymphatic function.
“This is this first study to document that sleep fragmentation, in the absence of an underlying neurological or medical disorder, impairs glymphatic function.”
Quote in the paperSubstantial claim - Premisecitation
SF 30 days treatment did not trigger any arteriole remodeling evident to immunolabeling against a-SMA and laminin.
“This is supported by our recent finding that SF 30 days treatment increased the density of the cortical microvasculature, but did not trigger any arteriole remodeling evident to immunolabeling against a-SMA (a-smooth muscle actin) and laminin.29”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [29]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Premisecitation
SF 30 days treatment increased the density of the cortical microvasculature.
“This is supported by our recent finding that SF 30 days treatment increased the density of the cortical microvasculature, but did not trigger any arteriole remodeling evident to immunolabeling against a-SMA (a-smooth muscle actin) and laminin.29”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [29]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Interpretationown data
AQP4 is unlikely involved in SF-induced suppression of glymphatic flow.
“However, we saw only minor changes in AQP4 polarization in SF 30 days mice versus control (Figure 5), rendering it unlikely that AQP4 is involved in SF-induced suppression of glymphatic flow.”
Quote in the paperSubstantial claim - Interpretationcitation
The results substantiate the established linkage between chronic insomnia and vascular pathologies, including vascular dementia.
“The results substantiate the established linkage between chronic insomnia and vascular pathologies, including vascular dementia.78,79”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [78]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [79]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Premisecitation
Central norepinephrine signaling is a key element in the regulation of glymphatic function.
“Indeed, central norepinephrine signaling is a key element in the regulation of glymphatic function.”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [3]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- Premisecitation
Extracellular norepinephrine levels drop abruptly upon the onset of REM sleep.
“Extracellular norepinephrine levels drop abruptly upon the onset of REM sleep.72”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [72]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- It may state two separate claims as one. 26
- Probably not a substantial claim. 27
It may state two separate claims as one.
Findingown dataThe reduction in tracer intensity and influx area was significant in subregions of cortex and subcortex, but not in hippocampus.
“This reduction was significant in subregions of cortex and subcortex, but not in hippocampus (Figure 3c-d).”
Quote in the paperNot a substantial claimIt may state two separate claims as one.
Findingown dataChronic sleep fragmentation suppresses slow vasomotion without altering cardiac-driven pulsations.
“A mechanistic analysis showed that the chronic sleep fragmentation suppressed slow vasomotion, without altering cardiac-driven pulsations.”
Quote in the paperSubstantial claimIt may state two separate claims as one.
Findingown dataVascular pulsatility and slow vasomotion did not differ between SF 3 days mice and normal sleep controls.
“Vascular pulsatility and slow vasomotion did not differ between SF 3 days mice and normal sleep controls (Figure 4b).”
Quote in the paperNot a substantial claimIt may state two separate claims as one.
Findingown dataSF 3 days and SF 30 days interventions both resulted in a significant reduction in the time fraction spent exploring the novel object compared with respective controls.
“Herein, NOR test consistently revealed that SF 3 days and SF 30 days interventions both resulted in a significant reduction in the time fraction spent in exploring the novel object in comparison with respective controls (Figure 1b-d).”
Quote in the paperSubstantial claimIt may state two separate claims as one.
Findingown dataThere was a striking dampening of slow vasomotion in SF 30 days group relative to their control group, but not in the SF 3 days group.
“In contrast, we saw a striking dampening of slow vasomotion in SF 30 days group relative to their control group, but not in the SF 3 days group.(Figure 4).”
Quote in the paperSubstantial claimIt may state two separate claims as one.
Findingown dataSleep fragmentation induces cognition decline and anxiety-like behaviors.
“Figure 1 . Figure 1.Sleep fragmentation induces cognition decline and anxiety-like behaviors.”
Quote in the paperSubstantial claimIt may state two separate claims as one.
Findingown dataChronic sleep fragmentation slightly alters the perivascular AQP4 distribution and enhances theta prevalence.
“Figure 5 . Figure 5. Chronic sleep fragmentation slightly alters the perivascular AQP4 distribution and enhances theta prevalence.”
Quote in the paperNot a substantial claimIt may state two separate claims as one.
Interpretationown dataSlow vasomotion, but not cardiac-driven arterial pulsatility, is suppressed by chronic sleep fragmentation.
“We thus draw the conclusion that slow vasomotion, but not cardiacdriven arterial pulsatility, is suppressed by chronic sleep fragmentation, which would imply that that repetitive sleep interruptions perturb cerebrovascular dynamics.”
Quote in the paperSubstantial claimProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
PremisecitationAutonomic arousal during NREM sleep generates a transient decrease in CBV, which promotes CSF pulsation on a slower time scale.
“Similar to the hemodynamic response driven by neural activity, autonomic arousal during NREM sleep generates a transient decrease in CBV, which also promotes CSF pulsation, albeit on a slower time scale.41”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [41]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim.
PremisecitationArterial wall elasticity and pulsatility decrease with aging and in pathologic conditions such as hypertension.
“Arterial wall elasticity and pulsatility are known to decrease with aging and in pathologic conditions such as hypertension.[20][21][22]”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [20]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [21]
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- cites [22]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
InterpretationcitationCSF flow could be driven by multiple mechanisms that change vascular volume.
“but it seems likely that CSF flow could be driven by the multiple mechanisms that change vascular volume.65”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [65]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
PremisecitationSlow vasomotion, along with pulsatility, contributes to driving CSF flow.
“Recent findings suggested that slow vasomotion, along with pulsatility, contributes to driving CSF flow.23,24”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [23]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [24]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
PremisecitationGlymphatic function is impaired in patients with neurodegenerative diseases and in experimental mouse models of Alzheimer's disease and Parkinson's disease.
“Numerous studies have shown that the glymphatic function is impaired in patients suffering from neurodegenerative diseases, as well as in experimental mouse models of Alzheimer's disease and Parkinson's disease.[15][16][17][18][19]”
Quote in the paperNot a substantial claim0 of 5 sources checked- cites [15]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [16]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [17]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [18]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [19]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
It may state two separate claims as one.
Interpretationown dataChronic sleep fragmentation in mice lasting 30 days led to cognitive impairments and anxiety-like behaviors, consistent with prior reports.
“In this study, chronic sleep fragmentation in mice lasting 30 days led to cognitive impairments and anxietylike behaviors, consistent with prior reports 13,43 (Figure 1).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [13]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [43]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
It may state two separate claims as one.
Interpretationown dataChronic sleep fragmentation significantly decreased CSF influx into the brain, as well as CSF efflux to the cervical lymph nodes, pointing to a global suppression of brain fluid flow.
“Focusing on glymphatic transport, we found that chronic sleep fragmentation significantly decreased CSF influx into the brain, as well as CSF efflux to the cervical lymph nodes, pointing to a global suppression of brain fluid flow (Figure 3).”
Quote in the paperSubstantial claimIt may state two separate claims as one.
Interpretationown dataSleep fragmentation for 30 days drastically suppressed spontaneous vasomotion, but not cardiac cycle-related pulsatility, in cortical arterial vessels in awake mice.
“The data thus suggest that sleep fragmentation for 30 days drastically suppressed spontaneous vasomotion, but not cardiac cycle-related pulsatility, in cortical arterial vessels in awake mice.”
Quote in the paperSubstantial claimProbably not a substantial claim. It may state two separate claims as one.
PremisecitationStress responses involve increased norepinephrine release and dysregulation of the hypothalamic-pituitary-adrenal (HPA) axis.
“Classically, stress responses involve increased norepinephrine release and dysregulation of hypothalamic-pituitary-adrenal (HPA) axis.”
Quote in the paperSubstantial claim0 of 2 sources checked- cites [67]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [68]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
PremisecitationEpidemiological studies have documented a strong association between chronic stress and cardiovascular diseases.
“Indeed, epidemiological studies have previously documented a strong association between chronic stress and cardiovascular diseases.70,71”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [70]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [71]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
Study design and conductown dataThere was no mortality in any experimental group, including mice exposed to chronic sleep fragmentation.
“There was no mortality in any of the experimental groups, including mice exposed to chronic sleep fragmentation.”
Quote in the paperNot a substantial claimIt may state two separate claims as one.
PremisecitationThe cardiac cycle and slow vasodynamics are the two major drivers of glymphatic transport.
“The cardiac cycle and slow vasodynamics are the two major drivers of glymphatic transport.”
Quote in the paperSubstantial claimIt may state two separate claims as one.
Interpretationown dataSF 3 days and SF 30 days treatment both induced cognitive impairment in young adult wildtype mice.
“In summary, SF 3 days and SF 30 days treatment both induced cognitive impairment in young adult wildtype mice.”
Quote in the paperSubstantial claimProbably not a substantial claim. The paper’s conclusions may not depend on it.
Study design and conductnone givenTracer influx was quantified by a blinded investigator.
“Tracer influx was quantified by a blinded investigator using Fiji/Image J software (NIH, USA).”
Quote in the paperNot a substantial claimProbably not a substantial claim. The paper’s conclusions may not depend on it.
Study design and conductnone givenApproximately 50 cortical blood vessels per mouse were randomly selected for AQP4 quantification.
“We randomly selected approximately 50 cortical blood vessels per mouse for quantification.”
Quote in the paperNot a substantial claimProbably not a substantial claim. The paper’s conclusions may not depend on it.
PremisereasoningThese drivers together initiate low-pressure gradients that propel peri-arterial CSF inflow to the brain parenchyma.
“These drivers together initiate low-pressure gradients that propel peri-arterial CSF inflow to the brain parenchyma.”
Quote in the paperNot a substantial claimIt may state two separate claims as one.
InterpretationreasoningBlood pressure and heart rate were likely unaffected at the end of SF 30 days interventions.
“Therefore, we suspect that blood pressure and heart rate were likely unaffected at the end of SF 30 days interventions.”
Quote in the paperNot a substantial claimProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
PremisecitationHypothalamic release of corticotropin-releasing factor elicits pituitary release of adrenocorticotropic hormone and consequential release of cortisol and catecholamines from the adrenal gland.
“Hypothalamic release of corticotropin-releasing factor elicits pituitary release of adrenocorticotropic hormone and the consequential release of cortisol and catecholamines from the adrenal gland.67,68”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [67]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [68]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
PremisecitationIn human and rodent brains, slow vasomotion falls within a broad range of frequencies centered around 0.1 Hz.
“In human and rodent brains, slow vasomotion falls within a broad range of frequencies centered around 0.1 Hz. 24”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [24]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
PremisecitationAnother group reported a transient increase in heart rate confined to the initial weeks of sleep fragmentation.
“They also reported a transient increase in heart rate confined to the initial weeks of sleep fragmentation.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [66]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
Study design and conductcitationVessel diameter changes exceeding 45% of baseline were excluded as likely motion artefacts.
“Applying the criteria from the prior study, 23 we excluded vessel diameter changes exceeding 45% of the baseline measurements as likely motion artefacts.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [23]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
Premisenone givenArterial pulsations are an important driving force for perivascular CSF flow, a key component of glymphatic function.
“Growing evidence highlights the importance of arterial pulsations as the driving force for perivascular CSF flow, a key component of glymphatic function.”
Quote in the paperNot a substantial claimIt may state two separate claims as one.
PremisecitationClearance of brain interstitial waste by the glymphatic system occurs primarily during sleep, driven by multiple oscillators including arterial pulsatility and vasomotion.
“Clearance of brain interstitial waste by the glymphatic system occurs primarily during sleep, driven by multiple oscillators including arterial pulsatility, and vasomotion.”
Quote in the paperSubstantial claim0 of 4 sources checked- cites [3]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [14]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [23]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [24]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
It may state two separate claims as one.
Interpretationown dataChronic sleep fragmentation suppresses brain metabolite clearance and impairs cognition even in the absence of disease.
“Taken together, results of this study document that chronic sleep fragmentation suppresses brain metabolite clearance and impairs cognition, even in the absence of disease.”
Quote in the paperSubstantial claimProbably not a substantial claim. The paper’s conclusions may not depend on it.
PremisecitationChronic overactivation of the HPA axis could lead to increased arterial stiffness and atherosclerosis.
“A chronic overactivation of the HPA axis could lead to increased arterial stiffness and atherosclerosis.67,69”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites [67]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [69]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
It may state two separate claims as one.
Interpretationown dataAcute and chronic sleep deprivation lack effect on BBB permeability.
“The analysis showed that neither SF 3 days nor SF 30 days treatments altered Evans Blue uptake relative to control mice, indicating a lack of effect of acute and chronic sleep deprivation on BBB permeability.”
Quote in the paperSubstantial claimIt may state two separate claims as one.
PremisecitationIn mice, slow vasomotion has much lower frequency (~0.1 Hz) than cardiac pulsatility (~5-10 Hz), but slow vasomotion evokes much larger amplitude changes in vascular diameter (10-15%) compared to cardiac pulsation (2-4%).
“In mice, slow vasomotion has much lower frequency ($0.1 Hz) than cardiac pulsatility ($5-10 Hz), but slow vasomotion evokes much larger amplitude changes in vascular diameter (10-15%) compared to cardiac pulsation (2-4%).20,23,37”
Quote in the paperSubstantial claim0 of 3 sources checked- cites [20]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [23]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [37]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
It may state two separate claims as one.
Interpretationown dataSF for 30 days significantly suppressed glymphatic influx into the brain, CSF efflux via the dCLNs and Ab1-40 clearance from prefrontal cortex, suggesting an overall impairment of CSF transport.
“In summary, SF for 30 days significantly suppressed glymphatic influx into the brain, CSF efflux via the dCLNs and Ab1-40 clearance from prefrontal cortex, suggesting an overall impairment of CSF transport.”
Quote in the paperSubstantial claimProbably not a substantial claim. The paper’s conclusions may not depend on it.
PremisecitationA non-significant trend towards increased blood pressure after SF 30 days compared with controls was recently reported.
“We recently reported that non-significant trend towards an increased blood pressure after SF 30 days compared with controls.29”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [29]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
PremisecitationAnother group found a minor but significant blood pressure increase after 8 weeks of sleep fragmentation.
“Another group using the same model found a minor but significant blood pressure increase after 8 weeks of sleep fragmentation.66”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [66]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
It may state two separate claims as one.
InterpretationreasoningChronic sleep fragmentation induces suppression of slow vasomotion, which in turn impairs glymphatic fluid transport in young, healthy wildtype mice.
“The present observations indicate that chronic sleep fragmentation induces suppression of slow vasomotion, which in turn impairs glymphatic fluid transport in young, healthy wildtype mice.”
Quote in the paperSubstantial claimProbably not a substantial claim. The paper’s conclusions may not depend on it.
PremisecitationCSF tracer influx and clearance of tracers injected into the brain are suppressed in AQP4 knockout mice.
“Polarized AQP4 expression is a fundamental requirement for intracerebral fluid transport, since CSF tracer influx and clearance of tracers injected into the brain are suppressed in AQP4 knockout mice.14,74,75”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites [14]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [74]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [75]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
PremisecitationPolarized AQP4 expression is a fundamental requirement for intracerebral fluid transport.
“Polarized AQP4 expression is a fundamental requirement for intracerebral fluid transport, since CSF tracer influx and clearance of tracers injected into the brain are suppressed in AQP4 knockout mice.14,74,75”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites [14]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [74]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [75]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
PremisecitationAQP4 polarization is under dynamic circadian regulation, which peaks at the zenith of glymphatic function during the behaviorally inactive phase.
“A recent study reported that AQP4 polarization is under dynamic circadian regulation, which peaks at the zenith of glymphatic function during the behaviorally inactive phase. 2”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [2]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
It may state two separate claims as one.
PremisecitationChronic sleep fragmentation significantly reduced the total duration of REM sleep, but not the duration of NREM sleep and wakefulness.
“Interestingly, our previous data showed that chronic sleep fragmentation significantly reduced the total duration of REM sleep, but not the duration of NREM sleep and wakefulness.29”
Quote in the paperSubstantial claim0 of 1 sources checked- cites [29]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
Study design and conductnone givenThe exclusive use of male mice limits the generalizability of present results.
“Our exclusive use of male mice limits the generalizability of present results.”
Quote in the paperNot a substantial claimProbably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
PremisecitationIn anesthetized mice, cortical EEG slow delta prevalence correlated strongly with glymphatic influx, while beta prevalence correlated inversely with glymphatic influx, with a trend towards a positive correlation for theta prevalence.
“Thus, cortical EEG slow delta prevalence correlated strongly with glymphatic influx, while beta prevalence correlated inversely with glymphatic influx in anesthetized mice, with a trend towards a positive correlation for theta prevalence.35”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [35]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
PremisecitationTheta burst stimulation facilitates glymphatic clearance efficiency after sleep deprivation.
“However, theta burst stimulation have been shown to facilitate glymphatic clearance efficiency after sleep deprivation.73”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [73]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
PremisecitationReduced vascular polarization of AQP4 in astrocytic endfeet is associated with declining CSF inflow.
“Other studies have shown that reduced vascular polarization of AQP4 in astrocytic endfeet is associated with declining CSF inflow.21,76,77”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites [21]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [76]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
- cites [77]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
Probably not a substantial claim. The paper’s conclusions may not depend on it.
PremisecitationNeural activity modulates glymphatic fluid transport.
“Neural activity has also been shown to modulate glymphatic fluid transport.35”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites [35]
Couldn’t be matched to a paper in Crossref, so it can’t be checked.
The paper relies on this without support.
It remains unknown how chronic sleep disturbances alter glymphatic function in young healthy animals, and whether vascular dysfunction links sleep disturbances with glymphatic decline.
“However, it remains unknown how chronic sleep disturbances alter glymphatic function in young healthy animals, and whether vascular dysfunction links sleep disturbances with glymphatic decline.”
The paper relies on this without support.
It remains unknown how chronic sleep disturbances in isolation from an underlying neurological disease may affect the glymphatic system.
“However, it remains unknown how chronic sleep disturbances in isolation from an underlying neurological disease may affect the glymphatic system.”
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Chronic sleep fragmentation impairs both slow vasomotion and glymphatic function.
“chronic sleep fragmentation impairs both slow vasomotion and glymphatic function77.”
From Norepinephrine-mediated slow vasomotion drives glymphatic clearance during sleep (2025) · cites this paper as [77]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
Each contradiction between two passages listed here was confirmed by an independent check.
Prior theta correlation given opposite directions
MinorTwo passages describing the prior anesthesia findings give opposite directions for the reported trend in the correlation between theta prevalence and glymphatic influx.
“Previous studies have shown that anesthesia increases glymphatic influx as a function of EEG delta prevalence, but with a weak trend towards a negative correlation for theta prevalence.35”
“Thus, cortical EEG slow delta prevalence correlated strongly with glymphatic influx, while beta prevalence correlated inversely with glymphatic influx in anesthetized mice, with a trend towards a positive correlation for theta prevalence.35”
Funding statement conflicts with grant acknowledgements
MinorThe acknowledgements say the work was supported by several grants, whereas the funding statement says the authors received no financial support for the research.
“This work was supported by the ministry of science and technology China Brain Initiative grant (2022ZD0204704), National Key R&D Program of China, 2021YFC2502200, the National Nature Science Foundation of China [grant numbers 81801318], and Shanghai Scientific Society, General Project [grant number 20ZR1403500, 21QA1401100].”
“The author(s) received no financial support for the research, authorship, and/or publication of this article.”
Theta increase described as both significant and a trend
MinorThe results call the increase in theta prevalence statistically significant, but the discussion describes that increase as a trend.
“Present results for the EEG power spectrum density recorded at ZT 5-12 showed that theta prevalence was significantly higher in SF 30 days mice than in normal sleep controls.”
“The implications of a trend towards an increased theta wave prevalence for glymphatic fluid transport are unknown.”
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Metadata
- Authors
- Deng, S., Hu, Y., Chen, S., Xue, Y., Yao, D., Sun, Q., Nedergaard, M., Wang, W., & Ding, F.
- Affiliations
- Shanghai Medical College of Fudan University (CN)
- First Affiliated Hospital Zhejiang University (CN)
- Tongji Hospital (CN)
- University of Copenhagen (DK)
- Corresponding author
- Wang, Wei
- Ding, Fengfei
- Venue
- Journal of Cerebral Blood Flow & Metabolism
- Publisher
- SAGE Publications
- Published
- 2024-04-19
- Volume
- 44
- Issue
- 9
- Pages
- 1515-1531
- ISSN
- 0271-678X (ISSN-L)
- 1559-7016
- PMC
- PMC11418708
- OpenAlex
- W4394961827
- Semantic Scholar
- 48ef6a2f3add14cc6d18c5605bd03474eb8f0d38
- Cited by
- 52
- References
- 84
- Citations by year
- 2026: 33 · 2025: 18 · 2024: 1
- FWCI
- 13.03
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Cerebral Blood Flow & Metabolism (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, other-oa)
- Funders
- National Natural Science Foundation of China (81801318)
- Topics
- Health Sciences › Medicine › Clinical Neurology › Cerebrospinal fluid and hydrocephalus
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury and Neurovascular Disturbances
- Keywords
- sleep fragmentation, glymphatic system, arterial pulsatility, cognitive impairment, sleep deprivation
- MeSH terms
- Glymphatic System, Animals, Brain, Cognition, Male, Mice, Inbred C57BL, Sleep Deprivation, Mice
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