Although the majority of the social deprivation work with nonhuman primates focused on the effects of maternal deprivation via peer‐rearing studies, it is also important to understand whether peer deprivation alone without the experience of maternal deprivation would lead to any alterations in behavioral development. In the wild, social interactions with peers and other community members constitute an important part of primates’ lives. For example, by six months of age, rhesus monkeys spend only about 20% of their awake time with their mothers but spend the rest of the time with peers and other community members (Stevens et al., 2009).
Based on the proposition that growing up with only a mother without having opportunities to interact with other peers may be harmful for the developmental of social skills, Kempes and her colleagues (2008) compared two groups of rhesus monkeys. The first group was reared only by their mothers and were deprived of peer interactions for the first year of their life and subsequently placed in a peer group with monkeys that were raised in a naturalistic group. The second group was monkeys that were raised in a naturalistic setting with their mothers and peers. Peer‐deprived monkeys showed higher rates of submissive behavior, stereotypic behaviors and agonistic behaviors, and lower rates of grooming and sitting together with other monkeys (Kempes et al., 2008). These findings suggest that being raised only with a mother without having opportunities to interact with peers impacts the development of primates negatively.
Studying Temperament in Nonhuman Primates
Although most studies have examined the role of social isolation via “experimental manipulations” that deprived primates from certain social experiences, “naturally occurring” variations in primates’ temperament may also contribute to their experiences of social isolation and loneliness, which in turn may be associated with behavioral and health problems (Capitanio, 2017). One temperament that has been associated with experiences of social isolation in human work is behavioral inhibition. Behavioral inhibition refers to heightened negative reactivity in the presence of unfamiliar individuals and in unfamiliar situations (Fox et al., 2005). Although research on behavioral inhibition has originated from work with human infants (Kagan, 1989), there is evidence suggesting that it is not a uniquely human temperament (Capitanio, 2018).
In nonhuman primates, behavioral inhibition is typically assessed via the social separation paradigm (Capitanio, 2017) or the human intruder paradigm (Kalin, 2017). In the social separation paradigm, monkeys are separated from their mothers or their social group, and their distress and vocalizations in response to these separations are observed. Monkeys who show more heightened distress are considered “high reactive,” whereas those who show less distress are considered “less reactive.” More heightened reactivity to social separation in general has been linked with anxiety (Suomi et al., 2011). In the human intruder paradigm, the monkeys first experience a brief social separation from their social group. Following this separation, a human intruder enters the room and looks at the wall, without making any direct eye contract with the monkey. After this phase, the intruder turns back at the monkey and makes direct eye contract (see Suomi et al., 2011).
Using an adapted version of the human intruder paradigm with three‐ to four‐month‐old rhesus monkeys, Chun and Capitanio (2016) identified behaviorally inhibited monkeys based on three criteria: low emotionality in the first hour following relocation, high vigilance at the end of the 25‐hour separation, and a blunted cortisol response seven hours after relocation/separation. Compared to noninhibited Rhesus, behaviorally inhibited Rhesus were found to spend less time in proximity with their mothers and experience less grooming, even though there were no differences in time of contact with their mothers. Behaviorally inhibited Rhesus infants were also found to spend more time engaging in nonsocial behaviors, such as being alone, as juveniles but not as adults, suggesting that behavioral inhibition in infancy is at least relatively stable from infancy to adolescence. Likewise, duration of nonsocial behaviors was also stable from juvenile years to adulthood (Chun & Capitanio, 2016). These findings suggest that natural variations in behavioral inhibition may contribute to the extent to which Rhesus spend their time nonsocially or perhaps in isolation from other members of their social group.
Kalin and his colleagues conducted a series of studies with Rhesus to examine the neural underpinnings of behavioral inhibition, which they refer to as anxious temperament. They have shown that the central nucleus of the amygdala, anterior hippocampus, and orbitofrontal cortex are key components of a larger complex neural network that underlies anxious temperament (Fox et al., 2008; Fox & Kalin, 2014). For example, Rhesus with higher levels of temperamental anxiety were shown to display more elevated metabolic activity in the central nucleus of the amygdala and anterior hippocampus in stressful and non‐stressful contexts (Fox et al., 2008). Targeted lesions in these brain regions were shown to lead to reductions in temperamental anxiety, suggesting that these brain regions likely play a “causal role” in the expression of anxious temperament (Fox & Kalin, 2014). Given that such targeted lesion studies can only be conducted in animal work, these findings have important implications for our understanding of the causal role of specific brain regions in the expression of socially anxious behaviors.
Based on these findings, a key question is how do these brain regions play a causal role in the expression of anxious temperament? One possibility is that the central nucleus of the amygdala may play a role in the experience of fear and inhibition, whereas the anterior hippocampus and orbitofrontal cortex may regulate the expression of anxiety by providing contextual and regulatory information to the amygdala (Fox & Kalin, 2014). In support of this idea, it was found that the lesions in orbitofrontal cortex led to reduced anxiety (freezing behavior) through an effect on the extended amygdala (Fox et al., 2010). This may be because when orbitofrontal cortex does not send certain contextual messages to the amygdala, the amygdala does not respond to distress to the same extent. These findings suggest that these three brain regions embedded within a larger neural network may influence the expression of anxious temperament not only directly but through their connections with each other. An important implication of these findings for interventions is that treatments that target multiple brain regions associated with anxious temperament might be more effective in treating anxious temperament and preventing social isolation that may occur as a result of socially anxious behavior.
In adult Rhesus, another trait that has been linked with their social experiences is sociability or the tendency to affiliate (Capitanio et al., 2014). In nonhuman primates, high sociability is operationalized by high ratings on warmth and affiliation, and low ratings on solidarity. When studying Rhesus with low sociability, Capitanio and his colleagues (2014) hypothesized that there could be two types of low sociable Rhesus: those that were introverted and those that are lonely. Introverted animals were characterized as those that showed low social attainment and low social initiations, suggesting that they did not attempt to form social connections. On the other hand, lonely animals were those that showed low social attainment but demonstrated high social initiation as the sociable animals. Although the lonely animals showed more social initiations than the introverted animals, they were similar in the extent to which they engaged in complex social behaviors such as “contact” and “initiation of grooming.” In line with the findings with humans (Cacioppo & Hawkley, 2009), the lonely animals were more “sensitive to social threat” such that they showed greater social interest in the “safe” juvenile targets compared to the “risky” targets, whereas the high‐sociable and introverted monkeys did not demonstrate such a preference (see Capitanio, 2017). In another study, it was shown that Rhesus that showed greater perceived social isolation reflected by low sociability and high social threat sensitivity demonstrated a sympathetic nervous system gene expression associated with increased inflammation and reduced antiviral responses (Cole et al., 2015). These findings suggest that lonely Rhesus that frequently initiated interactions but could not succeed in social attainment were more sensitive to social threat and showed poorer health outcomes. In sum, individual differences in Rhesus’ temperamental characteristics such as behavioral inhibition and sociability emerge early in development and are relatively stable across time, and these temperamental characteristics may play a role
