Early-life sleep disruption increases parvalbumin in primary somatosensory cortex and impairs social bonding in prairie voles

Jones, Carolyn E.; Opel, Ryan A.; Kaiser, Mara E.; Chau, Alex Q.; Quintana, Jazmine; Nipper, Michelle A.; Finn, Deborah A.; Hammock, Elizabeth A. D.; Lim, Miranda M.

doi:10.1126/sciadv.aav5188

Cited by 55 publications

(142 citation statements)

References 61 publications

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“…REMS has also been shown to increase synaptic pruning in adolescent mice (Li, Ma, Yang, & Gan, 2017). Last, early life sleep deprivation has been shown to influence social bonding in adulthood (Jones et al, 2019). Overall these studies provide evidence that sleep contributes to brain development and that lack of sleep during early life may have long-lasting effects on human behavior.…”

Section: The Role Of Sleep In Brain Developmentmentioning

confidence: 72%

“…The timing of these events and the established role of GABA as the primary neurotransmitter of sleep promoting nuclei (Schwartz & Kilduff, 2015) raise the possibility that the development of inhibitory input into the cortex and the role of sleep in brain development are related. GABAergic interneuron development has been shown to be sensitive to sleep disruption in both kittens and young voles (Hogan, Roffwarg, & Shaffery, 2001;Jones et al, 2019). The role of sleep in forms of developmental synaptic plasticity dependent upon inhibitory circuits is well established (Frank et al, 2001).…”

Section: Is There a Link Between Abnormal Sleep Development And Asd?mentioning

confidence: 99%

“…NREMS enhances synaptic plasticity in the cortex of kittens (Frank et al, 2001) One week of REMS deprivation in immature rats prolongs the critical period for developmentally regulated synaptic plasticity (Shaffery, Sinton, Bissette, Roffwarg, & Marks, 2002) Chronic sleep deprivation causes a decrease in hippocampal volume in adolescent rats (Novati, Hulshof, Koolhaas, Lucassen, & Meerlo, 2011) REMS enhances experience-dependent plasticity in developing cerebral cortex in kittens (Dumoulin Bridi et al, 2015) REMS prunes new formed postsynaptic dendritic spines in mouse motor cortex during development and after motor learning (Li et al, 2017) Pharmacological sleep deprivation in rats 1-3 weeks of age results in behavioral changes and sleep disturbances into adulthood (Mirmiran, 1986) Early life sleep disruption impairs social bonding (Jones et al, 2019) model is generated with the same underlying biological cause, for example, the targeted mutations in the animal model replicate the causal genetic variant in the patient population. Face validity ensures that the model's behavior is analogous to the symptoms of the human disease (Chadman, Yang, & Crawley, 2009).…”

Section: Nrems Remsmentioning

confidence: 99%

“…One possibility is that the underlying cellular and molecular abnormalities causal to ASD also produce abnormal sleep (i.e., abnormal sleep is one of many outcomes of an underlying problem). Considering the potential role of sleep in brain development and that early sleep disruption has been shown to impair social bonding in animal models (Jones et al, 2019), it is also possible that abnormal sleep plays a causal role in ASD. A third non-mutually exclusive possibility is that there is an interaction between the genetic variants linked to ASD and the role of sleep early in life, which influences both the presence of sleep problems and the severity of ASD.…”

Section: Introductionmentioning

confidence: 99%

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Sleep, brain development, and autism spectrum disorders: Insights from animal models

Wintler

Schoch

Frank

et al. 2020

J of Neuroscience Research

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Sleep is an evolutionarily conserved and powerful drive, although its complete functions are still unknown. One possible function of sleep is that it promotes brain development. The amount of sleep is greatest during ages when the brain is rapidly developing, and sleep has been shown to influence critical period plasticity. This supports a role for sleep in brain development and suggests that abnormal sleep in early life may lead to abnormal development. Autism spectrum disorder (ASD) is the most prevalent neurodevelopmental disorder in the United States. It is estimated that insomnia affects 44%–86% of the ASD population, predicting the severity of ASD core symptoms and associated behavioral problems. Sleep problems impact the quality of life of both ASD individuals and their caregivers, thus it is important to understand why they are so prevalent. In this review, we explore the role of sleep in early life as a causal factor in ASD. First, we review fundamental steps in mammalian sleep ontogeny and regulation and how sleep influences brain development. Next, we summarize current knowledge gained from studying sleep in animal models of ASD. Ultimately, our goal is to highlight the importance of understanding the role of sleep in brain development and the use of animal models to provide mechanistic insight into the origin of sleep problems in ASD.

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Section: The Role Of Sleep In Brain Developmentmentioning

confidence: 72%

Section: Is There a Link Between Abnormal Sleep Development And Asd?mentioning

confidence: 99%

Section: Nrems Remsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Sleep, brain development, and autism spectrum disorders: Insights from animal models

Wintler

Schoch

Frank

et al. 2020

J of Neuroscience Research

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“…We pursued this with evaluation of the expression of nrxn1, previously associated with social behavior, in brain regions known to be integral to the neurocircuitry of social interaction (amygdala, anterior cingulate cortex, somatosensory cortex). [42][43][44][45][46][47][48][49] Expression of nrxn1 was differentially regulated in the brain regions of OXT-exposed offspring regardless of the sex; nrxn1 was significantly downregulated in the amygdala, but unchanged in the anterior cingulate and the somatosensory cortices of OXT vs. control offspring. Because these results do not explain male-specific impairment of social behavior, we speculate that these changes could be due to sex differences in the response to oxidative stress.…”

Section: Discussionmentioning

confidence: 96%

Transient uterine hypercontractility causes fetal cerebral oxidative stress and enduring mitochondrial and behavioral abnormalities in adolescent male rat offspring

Palanisamy¹,

Giri²,

Jiang³

et al. 2019

Preprint

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The impact of transient ischemic-hypoxemic insults on the developing fetal brain is poorly understood despite evidence suggesting an association with neurodevelopmental disorders such as schizophrenia and autism. To address this, we designed an aberrant uterine hypercontractility paradigm with oxytocin to better assess the consequences of acute, but transient, placental ischemia-hypoxemia in term pregnant rats. Using MRI imaging, we confirmed that oxytocininduced aberrant uterine hypercontractility significantly compromised uteroplacental perfusion.This was supported by the observation of oxidative stress and increased lactate concentration in the fetal brain. Genes related to oxidative stress pathways were significantly upregulated in male, but not female, offspring 1 h after oxytocin-induced placental ischemia-hypoxemia. Persistent upregulation of select mitochondrial electron transport chain complex proteins in the anterior cingulate cortex of adolescent male offspring suggested that this sex-specific effect was enduring.Functionally, offspring exposed to oxytocin-induced uterine hypercontractility showed malespecific abnormalities in social behavior with associated region-specific changes in gene expression and functional cortical connectivity. Our findings, therefore, indicate that even transient but severe placental ischemia-hypoxemia could be detrimental to the developing brain and point to a possible mitochondrial link between intrauterine asphyxia and neurodevelopmental disorders. 8.2.1; GraphPad Software Inc.), behavioral data with SYSTAT12 (Chicago, IL), and fcOISI data with MATLAB. Study approval:All experiments reported here were approved by the Institutional Animal Care and Use Committee at Washington University in St. Louis (#20170010) and comply with the ARRIVE guidelines. Author contributionsAP conceived the study design, planned the experiments, and wrote the manuscript with help from all co-authors. AP, TG and JJ developed the OXT dosing paradigm and conducted the molecular biology experiments. JDQ and JRG performed the placental imaging experiments, analyzed the data, and helped draft the manuscript. SBC performed the behavioral experiments, and SEM and DFW conducted the analysis and helped with interpretation and drafting of the manuscript. AB and AQB collected, analyzed, and interpreted the fcOISI data, and helped write the manuscript.

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Critical periods shaping the social brain: A perspective from Drosophila

Dombrovski

Condron

2020

BioEssays

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Many sensory processing regions of the central brain undergo critical periods of experience-dependent plasticity. During this time ethologically relevant information shapes circuit structure and function. The mechanisms that control critical period timing and duration are poorly understood, and this is of special importance for those later periods of development, which often give rise to complex cognitive functions such as social behavior. Here, we review recent findings in Drosophila, an organism that has some unique experimental advantages, and introduce novel views for manipulating plasticity in the post-embryonic brain. Critical periods in larval and young adult flies resemble classic vertebrate models with distinct onset and termination, display clear connections with complex behaviors, and provide opportunities to control the time course of plasticity. These findings may extend our knowledge about mechanisms underlying extension and reopening of critical periods, a concept that has great relevance to many human neurodevelopmental disorders.

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Early-life sleep disruption increases parvalbumin in primary somatosensory cortex and impairs social bonding in prairie voles

Abstract: Sleep is critical for proper sensory and social development in young prairie voles, an affiliative and monogamous rodent species.

Cited by 55 publications

References 61 publications

Sleep, brain development, and autism spectrum disorders: Insights from animal models

Sleep, brain development, and autism spectrum disorders: Insights from animal models

Transient uterine hypercontractility causes fetal cerebral oxidative stress and enduring mitochondrial and behavioral abnormalities in adolescent male rat offspring

Critical periods shaping the social brain: A perspective from Drosophila

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