and/or spend their time in in isolation from others.
Rodent Models
Why Are Rodent Models Useful?
Although rodents are phylogenetically not as close to humans as primates are, they show many similarities to humans in terms of genetic background, anatomy, physiology, and social life. Given rodents’ shorter life cycle, they allow for examining the effects of early experiences within a couple of weeks, rather than decades. Similar to humans and primates, rodents spend the majority of their postnatal period in close care of their parents (Champagne et al., 2003), which provides opportunities to examine whether and how the absence of these early experiences can lead to disruptions in development. After weaning, most rodents spend a large proportion of their time with peers or other rodents in the community. Thus, their social nature also allows for examining the effects of deprivation of such critical experiences.
Effects of maternal separation and maternal deprivation in rodents.
Early studies of Levine (1960) followed by Meaney’s and his colleagues work (1988) have made a substantial impact to the study of maternal separation and deprivation in rodents. Levine designed one of the first postnatal paradigms used with rodents (i.e., handling) to manipulate the mother–infant relationship. In this paradigm, animals are temporarily removed from their mother and their litter and placed into individual cages for up to 15 minutes until their weaning period (Levine, 1960). Research has linked handling with a range of positive developmental outcomes. It leads to increased intensified maternal care involving licking and grooming behaviors as well as greater infant–mother social interactions, which provide the infant with increased sensory stimulation. This enhanced sensory stimulation, in return, has been shown to lead to increases in the secretion of growth hormones, serotonin and thyroid (Meaney et al., 1988). Compared to non‐handled animals, neonatally handled animals display increased exploration (Weinberg et al., 1978), lower levels of emotional reactivity and fearfulness, lower adrenocortical reactivity in response to novel stimuli, and better spatial learning and memory (Meaney et al., 1988). Likewise, handling has been associated with lower anxiety‐ and depression‐like behaviors in male mice (Liu et al., 1997). Overall, this body of work with rodents suggests that infants’ brief separations from the mother in early development are mostly associated with positive emotional and cognitive outcomes rather than negative outcomes. Brief separations are therefore often considered as “brief immunizations” that allow infants to deal with challenges in a less emotionally reactive and cognitively effective way.
In contrast to the positive effects of handling, longer separations from the mother during infancy have been shown to lead to problematic outcomes. Two main paradigms have been utilized to examine the effects of longer separations from the mother. In maternal separation paradigms, the animals are removed from the litter for about one to eight hours per day (Knop et al., 2017), whereas in social deprivation paradigms, animals are removed for longer durations up to 24 hours per day. Maternal separations for six to eight hours lead to hyper‐responsivity of the neuroendocrine system with increases in the production of neuroendocrine hormones such as corticosterone (Levine 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
