Early life sleep disruption potentiates lasting sex-specific changes in behavior in genetically vulnerable Shank3 heterozygous autism model mice

Lord, Julia S.; Gay, Sean M.; Harper, Kathryn M.; Nikolova, Viktoriya D.; Smith, Kirsten M.; Moy, Sheryl S.; Diering, Graham H.

doi:10.1186/s13229-022-00514-5

Cited by 22 publications

(28 citation statements)

References 61 publications

(165 reference statements)

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“…Single housed mice generate ~6500 bouts of rest and PA per day, this is in agreement with data for C57BL/6 obtained by a HCM system using force plates [44]. Eighty percent are bouts of PA corresponding to only ~20% of the file time (see also [45,46] later confirmed and extended by correlative assessment of home-cage periods of long rest using piezo-electric sensor [48], IR-sensor [20,49], CCD [21,22], and electric-field sensor [50] based HCM techniques combined with EEG-EMG recordings. The results of these studies show a correlation >0.9 between NREM and REM sleep, on the hand, and the animals being still ≥40s, on the other.…”

Section: Bouts Of Rest and Pasupporting

confidence: 86%

“…Pack et al [47] found by comparing EEG and EMG recording with CCD a >90% agreement between long periods of rest (CCD; ≥30s) and EEG-EMG pattern of NREM and REM sleep. These observations were later confirmed and extended by correlative assessment of home-cage periods of long rest using piezo-electric sensor[48], IR-sensor[20, 49], CCD[21, 22], and electric-field sensor [50] based HCM techniques combined with EEG-EMG recordings. The results of these studies show a correlation >0.9 between NREM and REM sleep, on the hand, and the animals being still ≥40s, on the other.…”

Section: Discussionmentioning

confidence: 84%

“…With GPS tracking becoming a more frequent feature of wearable devices also distance made and speedograms will be possible to retrieve as indices. Similarly, data generated by a variety of HCM systems have recently been used in efforts to identify behavioural indices of ageing[29, 83], impact of disease progression[42, 43, 60, 84, 85], genetic modification[44, 48, 51, 53, 86], and insults[59, 60, 87].…”

Section: Discussionmentioning

confidence: 99%

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Bouts of rest and physical activity in C57BL/6J mice

Pernold¹,

Rullman²,

Ulfhake³

2023

Preprint

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The objective was to exploit the raw data output from a scalable home cage (type IIL IVC) monitoring (HCM) system (DVC®), to characterize pattern of undisrupted rest and physical activity (PA) of C57BL/6J mice. The system's tracking algorithm show that mice in isolation spend 67% of the time in bouts of long rest (>=40s) and 59 % of the time was interpreted as sleep. Twenty percent is physical activity (PA), split equally between local movements and locomotion. Decomposition revealed that a day contains ~6500 discrete bouts of short and long rest, local and locomotor movements. Mice travel ~330m per day, mainly during the dark hours, while travelling speed is similar through the light-dark cycle. Locomotor bouts are usually <0.2m and <1% are >1m. Tracking revealed also fits of abnormal behaviour. The starting positions of the bouts showed no preference for the rear over the front of the cage floor, while there was a strong bias for the peripheral (75%) over the central floor area. The composition of bouts has a characteristic circadian pattern, however, intrusive husbandry routines increased bout fragmentation by ~40%. Extracting electrode activations density (EAD) from the raw data yielded results close to those obtained with the tracking algorithm, with 59% of time in long rest (<1 EAD s-1) and 20% in PA. We confirm that EAD correlates closely with movement distance (rs>0.95) and the data agreed in ~96% of the file time. Thus, albeit EAD being less informative it may serve as a proxy for PA and rest, enabling monitoring group housed mice. The data show that a change in housing density from one to two, and up to three mice had the same effect size on EAD (~2) with no difference between sexes. The EAD deviated significantly from this stepwise increase with 4 mice per cage, suggesting a crowdedness stress inducing sex specific adaptations. We conclude that informative metrics on rest and PA can be automatically extracted from the raw data flow in near-real time (< 1 hrs). These metrics relay useful longitudinal information to those that use or care for the animals.

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Section: Bouts Of Rest and Pasupporting

confidence: 86%

Section: Discussionmentioning

confidence: 84%

Section: Discussionmentioning

confidence: 99%

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Bouts of rest and physical activity in C57BL/6J mice

Pernold¹,

Rullman²,

Ulfhake³

2023

Preprint

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“…For example, sleep loss in mice during the visual CP impairs cortical plasticity necessary for normal development of binocular vision (Renouard et al, 2022, this issue;Zhou et al, 2020). Consistent with CPs in complex behavior, sleep disruption in early life leads to persistent alterations in social interactions and cognition in wild type rodents (voles) and in an autism mouse model (Jones et al, 2021(Jones et al, , 2019Lord et al, 2022;Milman et al, 2023). Collectively, these findings may explain why during the 3 rd -4 th postnatal week (when many CPs occur in rodents) SD impacts PFC gene expression in ways not found at other ages.…”

Section: Sd Induced Changes Unique To P24: a Window Of Vulnerability?mentioning

confidence: 99%

Ontogenesis of the molecular response to sleep loss

Muheim

Ford

Medina

et al. 2023

Preprint

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Sleep deprivation (SD) results in profound cellular and molecular changes in the adult mammalian brain. Some of these changes may result in, or aggravate, brain disease. However, little is known about how SD impacts gene expression in developing animals. We examined the transcriptional response in the prefrontal cortex (PFC) to SD across postnatal development in male mice. We used RNA sequencing to identify functional gene categories that were specifically impacted by SD. We find that SD has dramatically different effects on PFC genes depending on developmental age. Gene expression differences after SD fall into 3 categories: present at all ages (conserved), present when mature sleep homeostasis is first emerging, and those unique to certain ages in adults. Developmentally conserved gene expression was limited to a few functional categories, including Wnt-signaling which suggests that this pathway is a core mechanism regulated by sleep. In younger ages, genes primarily related to growth and development are affected while changes in genes related to metabolism are specific to the effect of SD in adults.

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“…The Shank3 mouse model is the only one in which sleep, and the impact of sleep loss has been examined early in life and in adults. Shank3 ΔC−/- have been shown to develop an abnormal response to sleep loss during the early developmental period ( Medina et al, 2022 ), while early-life sleep disruption in Shank3 ΔC−/+ has been shown to affect behavior in adulthood ( Lord et al, 2022 ). Mutations in Shank3 have also been shown to lead to deficits in homeostatic plasticity during the critical period, although those studies were done in a different mutant line ( Shank3B ) from the sleep studies ( Tatavarty et al, 2020 ).…”

Section: Introductionmentioning

confidence: 99%