Prolonged Maternal Separation Reduces Anxiety State and Increases Compulsive Burying Activity in the Offspring of BALB/c Mice

Jarrar, Qais; Ayoub, Rami; Alhussine, Kawther; Goh, Khang Wen; Moshawih, Said; Ardianto, Chrismawan; Goh, Bey Hing; Ming, Long Chiau

doi:10.3390/jpm12111921

Cited by 12 publications

(8 citation statements)

References 103 publications

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“…For example, brief maternal separation (15 min per day) was reported to reduce both anxiety- and depression-like behaviors in female C57BL/6J mice with imiquimod-induced psoriasis as evaluated using the sucrose preference and open field tasks ( Zhou et al, 2022 ). Additionally, adult male BALB/c mice that underwent maternal separation for 4 h per day were categorized as exhibiting anxiolytic behavior in the elevated plus maze and marble-burying tests ( Jarrar et al, 2022 ). These heterogeneous results may stem from differences in the duration and number of days of the maternal separation or differences in the mouse strains used.…”

Section: Discussionmentioning

confidence: 99%

Resveratrol ameliorates maternal separation-induced anxiety- and depression-like behaviors and reduces Sirt1-NF-kB signaling-mediated neuroinflammation

Wei

Zhang

Feng

et al. 2023

Front. Behav. Neurosci.

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Maternal separation in early life has a detrimental effect on the physiological and biochemical functions of the brains of offspring and can lead to anxiety- and depression-like behaviors later in life. Resveratrol possesses a variety of pharmacological properties, including anti-inflammatory, anxiolytic, and anti-depressive effects. In rodents, resveratrol can attenuate anxiety- and depression-like behaviors induced by chronic unpredictable mild stress, estrogen deficiency, and lipopolysaccharide. However, whether resveratrol administration during adolescence can counteract these behaviors when they result from maternal separation is unknown. In this study, male C57BL/6J mice were separated from their mothers for 4 h per day from postnatal day 2 (PND 2) to PND 21; starting on PND 61, resveratrol was administered intraperitoneally at 40 mg/(kg/day–1) for 4 weeks. At 3 months of age, anxiety and depression-like behaviors were assessed in the male offspring using a series of tasks consisting of an open field test, an elevated plus maze test, a forced swimming test, and a tail suspension test. The hippocampal levels of interleukin (IL)-1β, IL-6, and tumor necrosis factor-alpha (TNF-α) were measured by ELISA, while those of sirtuin 1 (Sirt1) and nuclear factor kappa B (NF-κB) p65 were determined by western blotting and PCR. The results showed that maternal separation led to increased anxiety- and depression-like behaviors, enhanced the levels of pro-inflammatory cytokines, and downregulated the Sirt1/NF-κB signaling pathway in the male offspring; however, these effects could be reversed by treatment with resveratrol. Our findings suggested that resveratrol can ameliorate inflammation and anxiety- and depression-like behaviors induced by maternal separation via the activation of the Sirt1/NF-κB pathway.

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Section: Discussionmentioning

confidence: 99%

Resveratrol ameliorates maternal separation-induced anxiety- and depression-like behaviors and reduces Sirt1-NF-kB signaling-mediated neuroinflammation

Wei

Zhang

Feng

et al. 2023

Front. Behav. Neurosci.

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“…Studies have also shown that an increase in ultrasonic vocalizations, which indicate anxiety-like behavior, occurs when maternal separation is performed in a different room (Kestering-Ferreira et al, 2021 ). However, anxiety-like behavior does not appear in cases where pups are not isolated in another room, such as by cross-fostering or transferring to a dam instead of pups (Luchetti et al, 2015 ; Jarrar et al, 2022 ). Our eDam group corresponds to the cross-fostering model, and the OF group corresponds to transferring the dam instead of the pups as the mother's scent remains in the cage.…”

Section: Discussionmentioning

confidence: 99%

The impact of environmental factors during maternal separation on the behaviors of adolescent C57BL/6 mice

Shin

Lee

2023

Front. Mol. Neurosci.

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Neonatal maternal separation is a widely used method to construct an early-life stress model in rodents. In this method, pups are separated from their mothers for several hours every day during the first 2 weeks of life, which results in adverse early-life events. It is a known fact that maternal separation can exert a significant impact on the behavior and psychological health, such as anxiety and depression, in adolescent offspring. However, environmental conditions during maternal separation can differ such as the presence of other animals or by placing pups in a different dam. To investigate the differential effects of various conditions of maternal separation on the behavior of adolescent mice, we created the following groups: (1) iMS group: pups were moved to an isolated room with no other adult mice in a nearby cage, (2) eDam group: the pups randomly exchanged their dams, (3) OF group: pups were shifted to another cage with the bedding material containing maternal odor (olfactory stimulation), and (4) MS group: pups were shifted to another vivarium. From postnatal day (PND) 2–20 (i.e., 19 consecutive days), pups were separated from the dam daily for 4 h and exposed to various environments (MS, iMS, eDam, and OF) or were left undisturbed [control (CON) group]. A series of behavioral assessments were conducted to evaluate locomotion, anxiety, recognition, learning, and memory in adolescent offspring. The results showed that neonatal maternal separation led to impaired recognition memory, motor coordination, and motor skill learning across all groups. However, the iMS group exhibited anxiety-like behavior in the elevated plus maze test and enhanced the extinction of fear memory in the auditory fear conditioning test. The OF and eDam groups displayed partially recovered short-term working memory in the Y-maze test but exhibited opposite exploratory behaviors. The OF group spent more time in the center, while the eDam group spent less time. These findings demonstrated that exposure to different environmental conditions during maternal separation causes behavioral alterations in adolescent offspring, providing a potential explanation for the variation in behavioral phenotypes observed in the early-life stress models.

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“…This maze is invested in predicting anxiolytic or anxiogenic activity (Jarrar et al, 2022). As seen in Table 7c, exposure to perovskite increased the time spent in each the light and dark compartments, the time spent to find the door, and the anxious index.…”

Section: Resultsmentioning

confidence: 99%

“…Furthermore, perovskite-treated mice demonstrated decreased marble burying activity than the controls suggesting anxiety-like behavior and exploring activities reduction (Arrant et al, 2013). Moreover, the behavior of perovskite-treated mice in the light and dark box maze may predict anxiolytic or anxiogenic activity (Bourin and Hascoet, 2003; Jarrar et al, 2022). Mice and rats exhibit burying activity when subjected to risky ambient environment (Angoe-Pereze et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

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Toxicity assessment of perovskite nanocomposites: In vivo study

Makableh,

Jarrar,

Al-Shdaifat

2023

Toxicol Ind Health

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Perovskite solar cells display potential as a renewable energy source because of their high-power conversion efficiency. However, there is limited understanding regarding the potential impact of perovskite on human health and the ecosystem. In this study, two sets of male Wistar albino rats received 35 injections of perovskite composite at a dosage of 0.372 mg/kg body weight. The animals underwent thorough examinations, encompassing morphometric, hematological, biochemical, histological, and behavioral analyses. Liver, kidney, and testis biopsies were processed and examined histologically. Additionally, two groups of mice (perovskite-treated and control mice, each with n = 10) underwent three behavioral tests: the Elevated Zero Maze test, Marble Burying test, and Light-Dark Box test. Perovskite-treated rats displayed a significant increase in levels of aspartate aminotransferase, alanine aminotransferase, alkaline phosphatase, triglycerides, cholesterol, creatinine, blood urea nitrogen, white blood cells, and platelets. However, total bilirubin levels decreased, with no significant alteration in albumin values. Furthermore, exposure to perovskite composite resulted in a slight decrease in lactate dehydrogenase and red blood cell count. Histopathological examination revealed hepatic hydropic degeneration, Kupffer cells hypertrophy and hyperplasia, and renal hydropic degeneration, while testicular tissues remained unaffected. Moreover, behavioral changes were observed in perovskite-treated mice, including depression, anxiety, and compulsive burying activity. These findings suggest that exposure to perovskite can lead to significant hematological and biochemical changes, as well as hepatorenal histopathological alterations and behavioral changes. Additionally, chronic exposure to perovskite materials may induce structural and functional alterations in vital organs.

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Prolonged Maternal Separation Reduces Anxiety State and Increases Compulsive Burying Activity in the Offspring of BALB/c Mice

Cited by 12 publications

References 103 publications

Resveratrol ameliorates maternal separation-induced anxiety- and depression-like behaviors and reduces Sirt1-NF-kB signaling-mediated neuroinflammation

Resveratrol ameliorates maternal separation-induced anxiety- and depression-like behaviors and reduces Sirt1-NF-kB signaling-mediated neuroinflammation

The impact of environmental factors during maternal separation on the behaviors of adolescent C57BL/6 mice

Toxicity assessment of perovskite nanocomposites: In vivo study

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