The Handbook of Solitude. Группа авторов
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The role of temperament in rodent social behaviors and social isolation.
Rodents’ temperament, particularly behavioral inhibition, has been linked with the extent to which they spend their time socially with others and health‐related outcomes. Cavigelli and her colleagues (2009) assessed rats’ behavioral inhibition based on their latency to approach to novelty in both social and nonsocial situations. In social situations, rats were introduced to a novel rat placed in a wired cage; in nonsocial situations, they were introduced to novel objects. They defined behavioral inhibition as longer than median latency to approach to novelty in social and nonsocial situations. Based on this definition, 30% of any tested group showed behavioral inhibition in both situations. Notably, rats’ responses to social situations and nonsocial situations were unrelated: rats could be slow to approach novel social situations but not slow at approaching novel objects. Latency to approach an object in the nonsocial condition was relatively stable across four months, whereas latency to approach an unfamiliar rat in the social condition was not stable over the same time period. Similar to findings in humans, about 17% of rats demonstrated a stable pattern of behavioral inhibition in social situations assessed four months apart, and these inhibited rats continued to show behavioral inhibition at a third time point (for a review see Cavigelli, 2018).
Importantly, behavioral inhibition predicted shortened life span (Cavigelli, 2018). Stable inhibition during social situations, however, was a better predictor of life span than inhibition during nonsocial situations, suggesting that wariness toward unfamiliar peers may be particularly detrimental to health and thus lead to shorter life spans (see Cavigelli, 2018). This may be because social wariness toward unfamiliar peers may increase stress levels, and lead to the “wear and tear” on the body. It is also possible that behaviorally inhibited rats may interact less with other rats and may not effectively use social partners to reduce their stress levels.
There is some evidence suggesting that behavioral inhibition leads to shorter longevity by altering the functioning of the neuroendocrine system. Behaviorally inhibited rats were shown to have 20–30% more basal glucocorticoids than noninhibited rats (Cavigelli et al., 2009), and greater levels of basal glucocorticoids in young adulthood predicted shorter life spans (Cavigelli et al., 2009). Notably, inhibition during social situations was a better predictor of basal glucocorticoid production and glucocorticoid reactivity than inhibition during nonsocial situations, suggesting that wariness in social situations may play an especially important role in altering the basal functioning of the neuroendocrine system. Behavioral inhibition was also associated with poorer cardiovascular system functioning (higher heart rate and blood pressure), which may be another mechanism by which behavioral inhibition may be linked with shorter life span (see Cavigelli, 2018). Finally, behavioral inhibition was associated with poor immune system functioning (an accentuated inflammatory response), which may also explain why this temperament trait may lead to shorter life span (see Cavigelli, 2018).
Although behavioral inhibition in infancy has been linked with greater basal glucocorticoid production and behavioral inhibition in later life, social experiences in adolescence were shown to moderate these associations (Caruso et al., 2014). Specifically, behaviorally inhibited rats that were housed with novel social partners in adolescence showed less exploratory behavior in adulthood compared to those housed with familiar social partners. On the other hand, behaviorally noninhibited rats that were housed with novel social partners in adolescence showed lower increase in basal glucocorticoid production and increased exploration in adulthood compared to rats that were housed with familiar rats. As such, rats that were noninhibited as infants displayed behaviors and physiology linked with behavioral inhibition. These findings suggested that relatively short‐term social experiences in adolescence may lead to changes in the stability of temperament as well as glucocorticoid production.
Conclusion and Future Directions
As reviewed in this chapter, nonhuman animal research has not only produced empirical findings that guide our understanding of how social deprivation and isolation impact developmental outcomes, but also played an important role in the formation of theories such as Bowlby’s attachment theory that have guided a fruitful body of research with humans. Although this chapter has primarily focused on nonhuman animal research, particularly Rhesus macaque. and rodents, there is also an extensive body of work examining the impact of social deprivation and social isolation in humans. For example, one form of social deprivation that is experienced by some children is growing up in institutional settings such as in orphanages. In such settings, children are often deprived of consistent and emotionally responsive caregivers due to factors such as high staff turn overs and rotations, high child to caregiver staff ratios, and insufficient staff training (Smyke et al., 2007). This form of social deprivation has been shown to have long‐lasting negative impact on children’s brain, social, and cognitive development (Hostinar et al., 2012; van Ijzendoorn et al., 2011). These findings are largely consistent with the nonhuman animal research findings reviewed in this chapter.
An important question that nonhuman animal researchers examined is to what extent the adverse impacts of early social deprivation are reversible when social deprivation is terminated. In human research, there is one project that was specifically designed to answer this question: the Bucharest Early Intervention Project (BEIP). The BEIP is a randomized control trial that examines whether children who are removed from institutional care and placed into a high‐quality foster care home show better developmental outcomes compared to those who have remained in the institutions, and equivalent or worse developmental outcomes compared to children who have never been institutionalized. Findings from this project show that children who receive the foster care intervention show better developmental outcomes compared to children who have remained in the institutions in certain areas such as social functioning and intelligence (see Nelson et al., 2019), suggesting that termination of severe social deprivation and transitioning to a responsive caregiving setting help boost the development in certain domains. Moreover, in certain developmental outcomes such as brain electrical activity, findings suggested that children who received the foster care intervention not only showed better developmental outcomes compared to the children who remained in the institutions, but also showed equivalent outcomes compared to those who have never been institutionalized (Debnath et al., 2020), suggesting that some of the adverse effects of institutional care may even be reversible. On the other hand, foster care intervention did not have a detectable positive effect on outcomes such as executive functions, which refers to goal‐directed cognitive skills (Wade et al., 2019). Thus, it might be that the effect of early social deprivation on such outcomes may not be reversible or may be reversible if children are removed within the first six months of development (Colvert et al., 2008). These findings are consistent with that of Harlow’s findings suggesting that the effects of early social deprivation are partially reversible depending on the duration of the social deprivation and timing of terminating social deprivation (Harlow & Suomi, 1971).
Although there is a good amount of human work examining the impact of institutional care or maternal deprivation on child outcomes, few studies have examined whether the impact of social deprivation or recovery from social deprivation depends on the child’s sex. Given the evidence from rodent work suggesting that there may be sex differences in whether or how well rodents recover from social deprivation after resocialization (Arakawa, 2007), it would be important to understand whether the impact of social deprivation or children’s recovery