findings suggest that although some responsibilities such as nest attendance were shared equally by parents, there were sex‐specific findings in the care of the offspring and partners when both partners were in the nest.
To test the effects of “paternal deprivation,” Ahern and his colleagues (2011) compared single‐mother and biparental households. They hypothesized that, to compensate for the absence of the paternal caregiving, single mothers would lick and groom their offspring more so than mothers in the biparental units. Contrary to this hypothesis, there were no differences in the extent to which single mothers and mothers in biparental units licked and groomed their pups. The absence of fathers had a large impact on the extent to which pups received parental care given that mothers did not compensate for the absence of paternal care. Compared to females reared by both parents, females reared without fathers licked and groomed their pups less especially when rearing them without a male partner, and displayed lower rates of alloparenting when presented with non‐descendant pups (Ahern & Young, 2009; Ahern et al., 2011). Both males and females raised without fathers were less likely to form normal pair‐bonding (Ahern & Young, 2009).
Research on the effects of paternal deprivation on offspring outcomes in mandarin voles yielded similar findings (Bales & Saltzman, 2016). Offspring reared without fathers displayed higher anxiety and reduced locomotor activity in an open field test (Jia et al., 2009), showed impaired social recognition (Cao et al., 2014), and displayed less social behavior and higher anxiety in a social interaction test (Jia et al., 2009). Males reared without fathers showed reduced play behaviors and more aggression toward unfamiliar females (Yu et al., 2012). Paternal deprivation had sex‐specific effects on the neuroendocrine system, such that paternally deprived females showed reduced glucocorticoid receptors and brain‐derived neurotrophic factor in the hippocampal formation, whereas males did not show such changes (Wu et al., 2014). Paternal deprivation also led to sex‐specific changes in the dopaminergic system: reduced mRNA expression of two dopamine receptors (type 1 & type 2) in female offspring in later life but enhanced expression of these receptors in males (Yu et al., 2012). Overall, findings from monogamous biparental rodent species suggest that paternal deprivation has effects on both the physiology and behavior of the offspring, but that these effects are often sex dependent.
Postweaning social isolation in rodents.
Both for humans and animals, social experiences that take place in childhood and adolescence play an important role for physical and mental health outcomes. In rodent work, the standard procedure used for examining the effects of social isolation in adolescence is the postweaning social isolation paradigm (Fone & Porkess, 2008). In this procedure, rodents are isolated from their dam and housed in individual cages on the first day of weaning typically until the day of testing. Isolation‐reared rats are housed in the same room as the control‐group rodents such that they can see, hear, and smell other rodents; however, they are prevented from socially interacting with them. Thus, this paradigm is designed to test whether deprivation from experiencing social interactions during the postweaning period without depriving pups from sensory stimuli (i.e., sight, auditory) impacts developmental outcomes.
Which developmental period does “postweaning” reflect? By the first day of weaning (postnatal day 20), rat cortex reaches 90% of the adult cortex. Children’s cortex reaches 90–95% of adult size by two to three years of age based on postmortem studies and around six years of age based on recent MRI work (Semple et al., 2013). Based on these estimates, the first days of weaning may correspond to the early childhood years. Notably, in rodent literature, the period from the first day of weaning to early adulthood is often referred to as adolescence (Lukkes et al., 2009). This period captures different developmental periods in rodents’ lives: puberty/preadolescence (postnatal day 21–28), early adolescence (pnd: 28–34), mid‐adolescence (pnd: 34–46) and early adulthood (pnd: 46–56; Lukkes et al., 2009). As such, the postweaning isolation studies aim to understand the extent to which the timing and duration of social isolation leads to lasting changes in rats’ biological systems as well as behavior.
The postweaning period reflects an important time for engaging in “social play” with litter mates and peers. Therefore, deprivation from opportunities to engage in “social play” is considered to be the main mechanism accounting for the effects of postweaning social isolation on rats’ behavior (Špinka et al., 2001). For example, although social isolation for the first 25 days after weaning led to heightened aggression and hyperarousal in novel environments, male rats that were allowed to have daily play bouts with a conspecific were protected from this effect (Einon et al., 1978; Potegal & Einon, 1989). Likewise, the effects of postweaning social isolation were not long‐lasting in species that do not typically engage in social play in adolescence (Lukkes et al., 2009). Thus, being deprived of social play may be a mechanism that can at least partially explain the effects of postweaning social isolation on rodents.
Postweaning social isolation was associated with both cognitive and emotional deficits. It was shown to lead to poor cognitive outcomes including impaired rule learning, recognition memory, and prepulse inhibition of acoustic startle (see Fone & Porkess, 2008), and resulted in reduced social interaction, increased aggression and antisociality, and anxiety‐like behaviors; though the effects depend on the timing and duration of the social isolation as well as the sex of the rodent (see Fone & Porkess, 2008). In both male and female rats, social isolation experienced from pre‐ to mid‐adolescence (about 15 days) led to increases in anxiety‐like behaviors including longer latency to emerge in an unfamiliar open‐field and reduced defensive burying reflecting lower levels of proactive coping (Arakawa, 2005, 2007). In males, the majority of these anxiety‐like behaviors did not disappear even after resocialization up to 90 days, suggesting that these behaviors are likely not reversible. Importantly, when male rats experienced the same duration of isolation in late adolescence, they did not show anxiety‐like behaviors. In contrast, in female rats, social isolation experienced in pre‐ to mid‐adolescence as well as experienced in adulthood led to anxiety‐like behaviors (Arakawa, 2007). These findings indicate that postweaning social isolation leads to poor developmental outcomes in both males and females. However, in females, these negative effects seem to be reversible by resocialization experiences, whereas, in males, certain developmental impairments may not be reversible by resocialization, suggesting that the adolescence period may constitute a critical period for the effects of social isolation in male rats.
Postweaning social isolation has been proposed to lead to anxiety‐like behaviors by disrupting the functioning of the neurotransmitter systems, specifically the serotonin and dopamine systems, which are known to modulate emotive behaviors and mental health systems (Lukkes et al., 2009). These systems follow a protracted course of development and are not fully developed until early to late adolescence. Postweaning social isolation has been shown to alter the functioning of these systems in a brain region‐specific manner. For example, it leads to increases in serotonergic activity in the medial prefrontal cortex, but decreases in in the hippocampus and decreases in the dopamine innervation in the medial prefrontal cortex but increases in dopaminergic activity in the NAc in male rats (see Lukkes et al., 2009). It is also possible that social isolation leads to deficits in behaviors by affecting the interactions between serotonin and dopamine functioning within the limbic system (Lukkes et al., 2009). For example, activation of the 5‐HT serotonin in the medial frontal cortex has been shown to lead to decreases in the dopamine release in this region. Thus, it is possible that rather than having a direct effect on both of these systems, postweaning social isolation may alter the functioning of one of these systems, which may in turn, lead to disruptions in the functioning of the other system.
Communal rearing as an enriched social environment in rodents.
The standard paradigm used to examine the impact of maternal caregiving on rodent pups’ development is housing the parent and her pups in one room in isolation from other rodents. However, under naturalistic conditions, rodent offspring are more typically reared by multiple female and sometimes male
