et al., 1991). Rats separated from their mothers for three hours per day showed greater alcohol dependency (drank more ethanol‐sucrose solution) than rats that were unseparated and those that were handled for 15 minutes per day (Huot et al., 2001). Longer durations of maternal separation and reduced maternal care lead to long‐term changes in the dopamine, oxytocin, and serotonergic systems, which in turn contribute to the observed increases in anxiety‐like and depression‐like behaviors (for a review, see Curley et al., 2011)
The lasting impact of maternal deprivation on developmental outcomes raises the question: what are the specific processes by which caregivers affect biology and behavior? Hofer (1978, 1994) suggested that mothers affect their offspring’s physiology via a multitude of “hidden regulatory processes” such as provision of milk, tactile stimulation, and warmth. Hofer and his students demonstrated that certain regulatory processes affect specific physiological or behavioral processes but not others (Hofer, 1987). For example, they examined the factors that may prevent two‐week‐old rat pups’ 40% reduction in heart rate in response to maternal separation. Although tactile stimulation or supplemental heat did not stop the reduction in heart rate, continuous infusion of milk into the pups’ stomach did maintain the heart rate at normative levels (Hofer, 1987; Hofer, 1971), suggesting that mothers regulate offspring’s heart rates mainly by providing milk. Hofer and his colleagues also showed that although infant rats experienced a reduction in their growth hormone secretion when separated from mothers, this response was prevented via rigorous tactile stimulation in the form of brush strokes, suggesting that mothers’ tactile stimulation may be the hidden process that facilitates normative levels of growth hormone secretion (Hofer, 2006). In another study, they demonstrated that the mere presence of an anesthetized mother who could not interact with the infant rat was sufficient to reduce neuroendocrine stress reactivity in response to novel stimuli, but the presence of food did not make the same impact (Stanton et al., 1988). Finally, rat pups that were kept in a warm environment after being deprived of maternal care and food continued to show normal activity level relative to those placed in cold environments (Stone et al., 1976). These findings suggest that there are multiple hidden regulatory processes by which mothers facilitate the growth and healthy functioning of their infant pups, and that specific regulatory processes may impact specific physiological and behavioral processes.
Effects of paternal deprivation in rodents.
Human family structures are diverse and complex. Some children are reared by their mothers and fathers, some are reared by two mothers or two fathers, while others are reared in single parent households. Some children are cared by their biological parents, some by their nonbiological parents while others are reared by a combination of both biological and nonbiological parents. Given the diversity in children’s experiences of family structure and parental care, it would be important to use animal models to understand the impact of deprivation from a specific type of caregiving, such as paternal caregiving, on offspring’s developmental outcomes.
Similar to work with humans, the majority of animal research has focused on the role of maternal parenting behaviors partly because most monkey and rodent species are reared primarily by their mothers. Fortunately, there are some rodent species including prairie voles (Microtus ochrogaster), Mandarin voles (Lasiopodomys mandarinus), and California mice (Peromyscus californicus) that are monogamous and display biparental parenting. For example, similar to humans, prairie voles maintain diverse family structures. In the wild, about one‐third of prairie vole pups are reared by their mothers and fathers, about one‐third are reared by single‐mothers, and about one‐third are reared in small communal groups with their biological parents and several alloparents (Getz & Carter, 1996). Interestingly, the majority of virgin female voles display “alloparental behavior” when placed with non‐descendent pups, suggesting that they also demonstrate the ability to take care of nonbiological offspring (see Bales & Saltzman, 2016). Given the diversity in their family structures and complex social behaviors, species such as prairie voles are excellent models for investigating the specific roles of mothers, fathers, as well as the impact of “biparenting” and “alloparenting.”
An important body of work examined the role of paternal deprivation on offspring outcomes in prairie voles. Ahern and his colleagues (2011) conducted a series of experiments to examine the sex‐specific parenting behaviors displayed in biparental family units and the effects of paternal deprivation on offspring outcomes. In biparental family units, mothers and fathers did not differ in the extent to which they attended to their nests, a behavior important for the protection of the offspring. Mothers and fathers licked and groomed their pups at similar rates when they were alone with their pups; however, mothers licked and groomed their pups more than fathers did when both parents were in the nest, whereas fathers demonstrated more partner‐directed licking and grooming than mothers did. These 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