Short-term sleep deprivation disrupts the molecular composition of ionotropic glutamate receptors in entorhinal cortex and impairs the rat spatial reference memory

Xie, Meilan; Li, Chao; He, Chao; Yang, Li; Tan, Gang; Yan, Jie; Wang, Jiali; Hu, Zhian

doi:10.1016/j.bbr.2015.10.002

Cited by 15 publications

(13 citation statements)

References 55 publications

(75 reference statements)

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“…Changes in GABA A Rs seen here can be likened to those seen in in vitro and in vivo studies, in which increased activity induced pharmacologically or by seizures resulted in increased GABA A Rs on the plasma membrane and correlated increases in IPSCs ( Nusser et al, 1998 ; Marty et al, 2004 ). Such homeostatic changes in receptors have been shown to occur within short time periods ( Yamanaka et al, 2000 ; Ibata et al, 2008 ; Xie et al, 2016 ), similar to the period of SD employed here. The GABA A Rs on the membrane of the RFMes GABA+ neurons returned to control levels here during increased sleep with SR, when according to the lack of c-Fos expression, the neurons were likely less active or inactive.…”

Section: Discussionsupporting

confidence: 61%

“…Collectively, these studies suggest that many cell groups which are normally active during waking and in a relative resting state during sleep undergo homeostatic regulation when submitted to enforced waking during the period when rodents normally sleep the majority of the time. Homeostatic changes associated with sleep and waking would include changes in glutamate as well as GABARs, which have been documented in the cortex and for which hypotheses and conclusions concerning Hebbian synaptic plasticity versus homeostatic synaptic scaling have diverged among scientists, and results have differed depending on the specific experimental paradigms and techniques employed ( Tononi and Cirelli, 2003 ; Vyazovskiy et al, 2008 ; Aton et al, 2009 ; Xie et al, 2016 ; Del Cid-Pellitero et al, 2017 ; Diering et al, 2017 ; Puentes-Mestril and Aton, 2017 ; Timofeev and Chauvette, 2017 ).…”

Section: Discussionmentioning

confidence: 99%

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Homeostatic Changes in GABA and Acetylcholine Muscarinic Receptors on GABAergic Neurons in the Mesencephalic Reticular Formation following Sleep Deprivation

Toossi

Cid-Pellitero

Jones

2017

eNeuro

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We have examined whether GABAergic neurons in the mesencephalic reticular formation (RFMes), which are believed to inhibit the neurons in the pons that generate paradoxical sleep (PS or REMS), are submitted to homeostatic regulation under conditions of sleep deprivation (SD) by enforced waking during the day in mice. Using immunofluorescence, we investigated first, by staining for c-Fos, whether GABAergic RFMes neurons are active during SD and then, by staining for receptors, whether their activity is associated with homeostatic changes in GABAA or acetylcholine muscarinic type 2 (AChM2) receptors (Rs), which evoke inhibition. We found that a significantly greater proportion of the GABAergic neurons were positively stained for c-Fos after SD (∼27%) as compared to sleep control (SC; ∼1%) and sleep recovery (SR; ∼6%), suggesting that they were more active during waking with SD and less active or inactive during sleep with SC and SR. The density of GABAARs and AChM2Rs on the plasma membrane of the GABAergic neurons was significantly increased after SD and restored to control levels after SR. We conclude that the density of these receptors is increased on RFMes GABAergic neurons during presumed enhanced activity with SD and is restored to control levels during presumed lesser or inactivity with SR. Such increases in GABAAR and AChM2R with sleep deficits would be associated with increased susceptibility of the wake-active GABAergic neurons to inhibition from GABAergic and cholinergic sleep-active neurons and to thus permitting the onset of sleep and PS with muscle atonia.

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Section: Discussionsupporting

confidence: 61%

Section: Discussionmentioning

confidence: 99%

Homeostatic Changes in GABA and Acetylcholine Muscarinic Receptors on GABAergic Neurons in the Mesencephalic Reticular Formation following Sleep Deprivation

Toossi

Cid-Pellitero

Jones

2017

eNeuro

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“…This is in contrast to other studies that have used longer periods (4–6 h) of total sleep deprivation and induced memory impairments [12,79–81]. Also, our lab has been able to produce significant memory loss using selective REM sleep deprivation for only 3 h [82].…”

Section: Discussionmentioning

confidence: 60%

Beyond Emotional and Spatial Processes: Cognitive Dysfunction in a Depressive Phenotype Produced by Long Photoperiod Exposure

2017

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Cognitive dysfunction in depression has recently been given more attention and legitimacy as a core symptom of the disorder. However, animal investigations of depression-related cognitive deficits have generally focused on emotional or spatial memory processing. Additionally, the relationship between the cognitive and affective disturbances that are present in depression remains obscure. Interestingly, sleep disruption is one aspect of depression that can be related both to cognition and affect, and may serve as a link between the two. Previous studies have correlated sleep disruption with negative mood and impaired cognition. The present study investigated whether a long photoperiod-induced depressive phenotype showed cognitive deficits, as measured by novel object recognition, and displayed a cognitive vulnerability to an acute period of total sleep deprivation. Adult male Wistar rats were subjected to a long photoperiod (21L:3D) or a normal photoperiod (12L:12D) condition. Our results indicate that our long photoperiod exposed animals showed behaviors in the forced swim test consistent with a depressive phenotype, and showed significant deficits in novel object recognition. Three hours of total sleep deprivation, however, did not significantly change novel object recognition in either group, but the trends suggest that the long photoperiod and normal photoperiod groups had different cognitive responses to total sleep deprivation. Collectively, these results underline the extent of cognitive dysfunction present in depression, and suggest that altered sleep plays a role in generating both the affective and cognitive symptoms of depression.

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“…Yet, the latter studies measured protein levels of the GluA1R in synaptoneurosomes of one cortical hemisphere by western blot and could not distinguish excitatory vs. inhibitory neurons, nor cell soma vs. dendrites or axons, nor differential trafficking of the receptor on or off the plasma membrane or synapse. On the other hand, another study which measured surface GluA1 and GluA2 subunits of the AMPA receptors in cortical neurons reported a decrease in surface expression of GluA1 subunits and an increase in that of GluA2 subunits after SD, indicating that GluA1-containing and GluA2-lacking, calcium-permeable AMPA receptors would be down-scaled during enforced waking with SD (Xie et al, 2016 ). In contrast using different techniques, studies examining the GluA1 and GluA2 subunits during dark vs. light periods of respective maximal wake vs. maximal sleep found somewhat different changes in synaptic AMPA receptors in cortex, likely in part due to the confounding of circadian and sleep processes (Lanté et al, 2011 ; Diering et al, 2017 ).…”

Section: Discussionmentioning

confidence: 99%

Homeostatic Changes in GABA and Glutamate Receptors on Excitatory Cortical Neurons during Sleep Deprivation and Recovery

Cid-Pellitero

Plavski

Mainville

et al. 2017

Front. Syst. Neurosci.

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Neuronal activity is regulated in a homeostatic manner through changes in inhibitory GABA and excitatory glutamate (Glu) AMPA (A) receptors (GluARs). Using immunofluorescent staining, we examined whether calcium/calmodulin-dependent protein kinase IIα (CaMKIIα)-labeled (+) excitatory neurons in the barrel cortex undergo such homeostatic regulation following enforced waking with associated cortical activation during the day when mice normally sleep the majority of the time. Sleep deprived mice were prevented from falling asleep by unilateral whisker stimulation and sleep recovery (SR) mice allowed to sleep freely following deprivation. In parallel with changes in c-Fos reflecting changes in activity, (β2-3 subunits of) GABAA Rs were increased on the membrane of CaMKIIα+ neurons with enforced waking and returned to baseline levels with SR in barrel cortex on sides both contra- and ipsilateral to the whisker stimulation. The GABAAR increase was correlated with increased gamma electroencephalographic (EEG) activity across conditions. On the other hand, (GluA1 subunits of) AMPA Rs were progressively removed from the membrane of CaMKIIα+ neurons by (Rab5+) early endosomes during enforced waking and returned to the membrane by (Rab11+) recycling endosomes during SR. The internalization of the GluA1Rs paralleled the expression of Arc, which mediates homeostatic regulation of AMPA receptors through an endocytic pathway. The reciprocal changes in GluA1Rs relative to GABAARs suggest homeostatic down-scaling during enforced waking and sensory stimulation and restorative up-scaling during recovery sleep. Such homeostatic changes with sleep-wake states and their associated cortical activities could stabilize excitability and activity in excitatory cortical neurons.

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Short-term sleep deprivation disrupts the molecular composition of ionotropic glutamate receptors in entorhinal cortex and impairs the rat spatial reference memory

Cited by 15 publications

References 55 publications

Homeostatic Changes in GABA and Acetylcholine Muscarinic Receptors on GABAergic Neurons in the Mesencephalic Reticular Formation following Sleep Deprivation

Homeostatic Changes in GABA and Acetylcholine Muscarinic Receptors on GABAergic Neurons in the Mesencephalic Reticular Formation following Sleep Deprivation

Beyond Emotional and Spatial Processes: Cognitive Dysfunction in a Depressive Phenotype Produced by Long Photoperiod Exposure

Homeostatic Changes in GABA and Glutamate Receptors on Excitatory Cortical Neurons during Sleep Deprivation and Recovery

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