Bratzu Jessica, Ciscato Maria, Pisanu Augusta, Talani Giuseppe, Frau Roberto, Porcu Patrizia, Diana Marco, Fumagalli Fabio, Romualdi Patrizia, Rullo Laura, Trezza Viviana, Ciccocioppo Roberto, Sanna Fabrizio, Fattore Liana
Neuroscience Institute, National Research Council of Italy (CNR), Cagliari, Italy.
Department of Biomedical Sciences, University of Cagliari, Monserrato, Italy.
Front Behav Neurosci. 2023 Oct 17;17:1257417. doi: 10.3389/fnbeh.2023.1257417. eCollection 2023.
Early social isolation (ESI) disrupts neurodevelopmental processes, potentially leading to long-lasting emotional and cognitive changes in adulthood. Communal nesting (CN), i.e., the sharing of parental responsibilities between multiple individuals in a nest, creates a socially enriching environment known to impact social and anxiety-related behaviors.
This study examines the effects of (i) the CN condition and of (ii) ESI during the 3 week of life (i.e., pre-weaning ESI) on motor, cognitive, and emotional domains during adolescence and adulthood in male and female rats reared in the two different housing conditions, as well as (iii) the potential of CN to mitigate the impact of ESI on offspring.
We found that in a spontaneous locomotor activity test, females exhibited higher activity levels compared to males. In female groups, adolescents reared in standard housing (SH) condition spent less time in the center of the arena, suggestive of increased anxiety levels, while the CN condition increased the time spent in the center during adolescence, but not adulthood, independently from ESI. The prepulse inhibition (PPI) test showed a reduced PPI in ESI adolescent animals of both sexes and in adult males (but not in adult females), with CN restoring PPI in males, but not in adolescent females. Further, in the marble burying test SH-ESI adolescent males exhibited higher marble burying behavior than all other groups, suggestive of obsessive-compulsive traits. CN completely reversed this stress-induced effect. Interestingly, ESI and CN did not have a significant impact on burying behavior in adult animals of both sexes.
Overall, our findings (i) assess the effects of ESI on locomotion, sensorimotor gating, and compulsive-like behaviors, (ii) reveal distinct vulnerabilities of males and females within these domains, and (iii) show how early-life social enrichment may successfully counteract some of the behavioral alterations induced by early-life social stress in a sex-dependent manner. This study strengthens the notion that social experiences during early-life can shape emotional and cognitive outcomes in adulthood, and points to the importance of social enrichment interventions for mitigating the negative effects of early social stress on neurodevelopment.
早期社会隔离(ESI)会扰乱神经发育过程,可能导致成年后出现持久的情绪和认知变化。群体筑巢(CN),即巢内多个个体分担育儿责任,创造了一个已知会影响社交和焦虑相关行为的丰富社交环境。
本研究考察了(i)CN条件以及(ii)出生后3周内的ESI(即断奶前ESI)对在两种不同饲养条件下饲养的雄性和雌性大鼠青春期和成年期的运动、认知和情感领域的影响,以及(iii)CN减轻ESI对后代影响的潜力。
我们发现在自发运动活动测试中,雌性大鼠的活动水平高于雄性。在雌性组中,饲养在标准饲养(SH)条件下的青少年在竞技场中心停留的时间较少,这表明焦虑水平增加,而CN条件增加了青少年期在中心停留的时间,但成年期没有,且与ESI无关。前脉冲抑制(PPI)测试显示,两性的ESI青少年动物以及成年雄性(但成年雌性没有)的PPI降低,CN恢复了雄性的PPI,但未恢复青少年雌性的PPI。此外,在大理石掩埋测试中,SH-ESI青少年雄性表现出比所有其他组更高的大理石掩埋行为,这表明具有强迫性特征。CN完全逆转了这种应激诱导的效应。有趣的是,ESI和CN对两性成年动物的掩埋行为没有显著影响。
总体而言,我们的研究结果(i)评估了ESI对运动、感觉运动门控和强迫样行为的影响,(ii)揭示了这些领域中雄性和雌性的不同脆弱性,以及(iii)表明早期生活中的社交丰富如何以性别依赖的方式成功抵消早期生活社交压力引起的一些行为改变。这项研究强化了早期生活中的社交经历可以塑造成年期情绪和认知结果的观念,并指出社交丰富干预对于减轻早期社交压力对神经发育的负面影响的重要性。