Effects of Maternal Deprivation and Complex Housing on Rat Social Behavior in Adolescence and Adulthood

Abstract

Early life context and stressful experiences are known to increase the risk of developing psychiatric disorders later in life, including disorders with deficits in the social domain. Our study aimed to investigate the influence of early life environment on social behavior in a well-controlled animal model. To this end we tested the effects of maternal deprivation (MD) on rat social play behavior in adolescence and social interaction in adulthood. Additionally, we provided a stimulating environment during adolescence (complex housing) as a potential intervention to diminish the effects of early life stress. Male and female Wistar rats were deprived from their mother for 24 h on postnatal day 3 (PND 3) or were left undisturbed. Complex housing started 5 days after weaning and consisted of housing 10 same-sex conspecifics in large, two-floor Marlau^TM cages until the end of the study. Social play behavior in adolescence was tested under different conditions (3 h vs. 24 h social isolation prior to testing). Maternally deprived males - but not females - showed a longer latency to play and a decreased total amount of social play behavior, after a 24 h isolation period. In adulthood, social discrimination was impaired in deprived male and female rats in the three-chamber social approach task. Complex housing did not moderate the effects of MD, but in itself induced a strong behavioral phenotype. Both complex housed males and females hardly displayed any play behavior after a 3 h isolation period. However, after 24 h of isolation, these animals showed shorter latencies to engage in social play behavior. Only complex housed males truly showed more social play behavior here, while showing less social interest in adulthood. We conclude that MD has mild negative effects on social behavior in adolescence and adulthood, which are not counteracted by complex housing. Complex housing induces a specific phenotype associated with rapid habituation; a lack of social play after short isolation periods, while increasing play behavior after a prolonged period of isolation in adolescence, and less social interest, paired with intact social discrimination in adulthood. In both early life settings, males seem to be more influenced by the early life environment compared to females.

Keywords: behavior; complex housing; early life stress; environmental enrichment; maternal deprivation; social play; three-chamber social approach task.

FIGURE 1

(A) Timeline of the experiments, (B) picture of the complex housing Marlau^TM cages for rats (manufactured by Viewpoint, France), and (C) Schematic representation of the three-chamber social approach task, containing a habituation, social interest, and social discrimination phase. During the social interest phase, an unfamiliar rat was placed in one of the cylinders, while the other cylinder remained empty. Rats are known to prefer exploring conspecifics over inanimate objects and this social preference was quantified with a discrimination index (DI) that indicates the percentage of time spent near the unfamiliar rat. During the social discrimination phase, the unfamiliar rat from the previous phase was now considered familiar and a new, unfamiliar rat was placed in the other cylinder. Given the choice between a familiar and unfamiliar rat, rats are expected to explore the unfamiliar stimulus rat. Social discrimination is represented with a DI that depicts the preference for the unfamiliar rat, i.e., the percentage of time spent near the unfamiliar rat.

FIGURE 2

Male adolescent social play behavior following 24 h of social isolation in maternally deprived (MD) and complex housed rats. (A) Total amount of pins, (B) latency to pin, (C) pin length, and (D) time spent in social exploration. Statistics depict main effects. Graphs represent mean + SEM. n = 10 play couples per experimental group.

FIGURE 3

Female adolescent social play behavior following 24 h of social isolation in MD and complex housed rats. (A) Total amount of pins, (B) latency to pin, (C) pin length, and (D) time spent in social exploration. Statistics depict main effects. Graphs represent mean + SEM. Group sizes: no-MD standard housing n = 13, no-MD complex housing n = 13, MD standard housing n = 13, MD complex housing n = 12 couples.

FIGURE 4

Male adult three-chamber social approach task in MD and complex housed rats. Social interest is represented by (A) the percentage of cylinder exploration time spent in the cylinder zone containing the unfamiliar rat and (B) the latency to approach both cylinders. Social discrimination is represented by (C) the percentage of cylinder exploration time spent in the cylinder zone containing the new unfamiliar rat and (D) the latency to approach both cylinders. Since activity declined over time, the 5-min task is split in two time bins in graphs A,C. Graphs represent mean + SEM. n = 16 males per experimental group. ^∗p < 0.05, ^∗∗p < 0.01, and ^∗∗∗p < 0.001 indicate that DI is significantly different from chance (tested with a one-sample Student’s t-test against 50%).

FIGURE 5

Female adult three-chamber social approach task in MD and complex housed rats. Social interest is represented by (A) the percentage of cylinder exploration time spent in the cylinder zone containing the unfamiliar rat and (B) the latency to approach both cylinders. Social discrimination is represented by (C) the percentage of cylinder exploration time spent in the cylinder zone containing the new unfamiliar rat and (D) the latency to approach both cylinders. Since activity declined over time, the 5-min task is split in two time bins. Graphs represent mean + SEM. Group sizes: no-MD standard housing n = 16, no-MD complex housing n = 12, MD standard housing n = 16, MD complex housing n = 15. ^∗p < 0.05, ^∗∗p < 0.01, and ^∗∗∗p < 0.001 indicate that DI is significantly different from chance (tested with a one-sample Student’s t-test against 50%).