Regulation of hippocampal dendritic spines following sleep deprivation

Gisabella, Barbara; Scammell, Thomas E.; Bandaru, Sathyajit S.; Saper, Clifford B.

doi:10.1002/cne.24764

Cited by 38 publications

(55 citation statements)

References 34 publications

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“…We speculate that diurnal molecular modifications of PNNs may contribute to memory formation and consolidation mechanisms during the wake/sleep cycle, favoring activity-driven synaptogenesis and synaptic refinement, respectively. For instance, our results on the effects of 5-h sleep deprivation on WFA1 PNNs in the mouse hippocampus are consistent with reports that 5 h of sleep deprivation prevents changes in dendritic spine densities in the hippocampus occurring during sleep (Havekes et al, 2016;Raven et al, 2019;Spano et al, 2019;Gisabella et al, 2020). PNN rhythms observed in our study may reflect ongoing systemic and synaptic consolidation during sleep proposed by Rasch and Born (Rasch and Born, 2013).…”

Section: Implications For Synaptic Plasticity and Memory Consolidationsupporting

confidence: 92%

Circadian Rhythms of Perineuronal Net Composition

Pantazopoulos

Gisabella

Rexrode

et al. 2020

eNeuro

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Perineuronal nets (PNNs) are extracellular matrix (ECM) structures that envelop neurons and regulate synaptic functions. Long thought to be stable structures, PNNs have been recently shown to respond dynamically during learning, potentially regulating the formation of new synapses. We postulated that PNNs vary during sleep, a period of active synaptic modification. Notably, PNN components are cleaved by matrix proteases such as the protease cathepsin-S. This protease is diurnally expressed in the mouse cortex, coinciding with dendritic spine density rhythms. Thus, cathepsin-S may contribute to PNN remodeling during sleep, mediating synaptic reorganization. These studies were designed to test the hypothesis that PNN numbers vary in a diurnal manner in the rodent and human brain, as well as in a circadian manner in the rodent brain, and that these rhythms are disrupted by sleep deprivation. In mice, we observed diurnal and circadian rhythms of PNNs labeled with the lectin Wisteria floribunda agglutinin (WFA1 PNNs) in several brain regions involved in emotional memory processing. Sleep deprivation prevented the daytime decrease of WFA1 PNNs and enhances fear memory extinction. Diurnal rhythms of cathepsin-S expression in microglia were observed in the same brain regions, opposite to PNN rhythms. Finally, incubation of mouse sections with cathepsin-S eliminated PNN labeling. In humans, WFA1 PNNs showed a diurnal rhythm in the amygdala and thalamic reticular nucleus (TRN). Our results demonstrate that PNNs vary in a circadian manner and this is disrupted by sleep deprivation. We suggest that rhythmic modification of PNNs may contribute to memory consolidation during sleep.

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Section: Implications For Synaptic Plasticity and Memory Consolidationsupporting

confidence: 92%

Circadian Rhythms of Perineuronal Net Composition

Pantazopoulos

Gisabella

Rexrode

et al. 2020

eNeuro

Self Cite

View full text Add to dashboard Cite

show abstract

“…We speculate that diurnal molecular modifications of PNNs may contribute to memory formation and consolidation mechanisms during the wake/sleep cycle, favoring activity-driven synaptogenesis and synaptic refinement, respectively. For instance, our results on the effects of 5 hour sleep deprivation on WFA+ PNNs in the mouse hippocampus are consistent with reports that 5 hours of sleep deprivation prevents changes in dendritic spine densities in the hippocampus occurring during sleep (Havekes et al, 2016;Raven et al, 2018;Spano et al, 2019;Gisabella et al, 2020). PNN rhythms observed in our study may reflect ongoing systemic and synaptic consolidation during sleep proposed by Rasch and Born (Rasch and Born, 2013).…”

Section: Implications For Synaptic Plasticity and Memory Consolidationsupporting

confidence: 92%

Circadian Rhythms of Perineuronal Net Composition

Pantazopoulos

Gisabella

Rexrode

et al. 2020

Preprint

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Perineuronal Nets (PNNs) are extracellular matrix (ECM) structures that envelop neurons and regulate synaptic functions. Long thought to be stable structures, PNNs have been recently shown to respond dynamically during learning, potentially regulating the formation of new synapses. We postulated that PNNs may vary during sleep, a period of active synaptic modification. Notably, PNN components are cleaved by matrix proteases such as the protease cathepsin-S, synthesized by microglia. Cathepsin-S is expressed in a diurnal manner in the mouse cortex, coinciding with dendritic spine density rhythms. Thus, cathepsin-S may induce PNN remodeling during sleep, mediating synaptic reorganization. These studies were designed to test the hypothesis that PNN numbers vary in a diurnal manner in the rodent and human brain, and in a circadian manner in the rodent brain, in association with cathepsin-S expression rhythms coinciding with reported rhythms in synaptic plasticity. In mice, we observed diurnal and circadian rhythms of PNNs labeled with the lectin wisteria floribunda agglutinin (WFA+PNNs) in several brain regions involved in emotional memory processing. Sleep deprivation prevented the daytime decrease of WFA+ PNNs. Diurnal rhythms of cathepsin-S expression in microglia were observed in the same brain regions, opposite to PNN rhythms. Finally, incubation of mouse sections with cathepsin-S eliminated PNN labeling. In humans, WFA+PNNs showed a diurnal rhythm in the amygdala and thalamic reticular nucleus (TRN). Our results demonstrate that PNNs vary in a circadian manner that coincides with expression rhythms of cathepsin-S in the mouse hippocampus. We suggest that rhythmic modification of PNNs may contribute to memory consolidation during sleep.

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“…We estimated that we had 25% (95% CI 22.25-27.70) power to detect a 15% (Glass’s delta 0.85) difference in dendritic spine density between sleep deprived and not sleep deprived mice, or a 63% (95% CI 60.13-66.20) power to detect a 30% difference (Glass’s delta 1.69). This can be put into contrast of the previously reported differences that has been in the range of 15-30% (Gisabella et al, 2020; Havekes et al, 2016).…”

Section: Resultscontrasting

confidence: 88%

Five hours total sleep deprivation does not affect CA1 dendritic length or spine density

Gabulya

Wellfelt

et al. 2021

Preprint

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Sleep is essential for long term memory function. However the neuroanatomical consequences of sleep loss are disputed. Sleep deprivation has been reported to cause both decreases and increases of dendritic spine density. Here we use Thy1-GFP expressing transgenic mice to investigate the effects of acute sleep deprivation on the dendritic architecture of hippocampal CA1 pyramidal neurons. We found that five hours of sleep deprivation had no effect on either dendritic length or dendritic spine density. Our work suggests that no major neuroanatomical changes result from one episode of sleep deprivation.

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Regulation of hippocampal dendritic spines following sleep deprivation

Cited by 38 publications

References 34 publications

Circadian Rhythms of Perineuronal Net Composition

Circadian Rhythms of Perineuronal Net Composition

Circadian Rhythms of Perineuronal Net Composition

Five hours total sleep deprivation does not affect CA1 dendritic length or spine density

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