affect their temperament, mood, and personality.
Harlow’s studies on maternal deprivation and total isolation.
Harry Harlow is one of the most prominent scientists who examined the effects of social deprivation and social isolation on nonhuman primates’ behaviors. Harlow strived to answer whether and how the type, duration, and the timing of social isolation had a lasting impact on rhesus monkeys’ behaviors. In his earlier studies, Harlow used the partial isolation paradigm: monkeys were separated from their mothers shortly after birth and kept alone in a wire‐meshed cage (see Harlow & Harlow, 1962). Although monkeys were kept alone in their cages, they were housed in a larger room where they could see and hear other monkeys but could not have direct physical contact with them. Harlow reported that monkeys that experienced partial isolation showed abnormal behaviors including staring blindly into space, engagement in repetitive and compulsive behaviors, and low levels of attention toward the monkeys kept in neighboring.
In subsequent studies, Harlow examined the effects of total isolation by removing monkeys from mothers shortly after birth and placing them into steel chambers that prevented them from seeing or hearing other monkeys or humans (Harlow et al., 1965). Harlow examined groups of monkeys that were kept in isolation for a duration of three months, six months, and one year, with the goal to understand if the duration of isolation had an effect on monkeys’ behaviors and whether it determined the “reversibility” of the early negative experiences. Harlow reported that the duration of social isolation had an additive or cumulative effect on later ability to socialize, such that monkeys isolated for three months showed noticeable disturbances in their social behaviors. However, those isolated for 6 months and 12 months showed increasingly worse social behaviors (Harlow et al., 1965). Harlow and his students also found that rhesus monkeys reared in total isolation for six months developed normal behavioral repertoire if they had opportunities to spend time with more socially skillful peers (Suomi & Harlow, 1972). These latter findings suggested that the maternally deprived monkeys’ behavioral problems were at least partially reversible if they had opportunities to interact with more socially competent peers.
Effects of peer‐rearing in nonhuman primates.
The effects of maternal deprivation on the development of primates is more commonly examined via peer‐rearing paradigms. In this paradigm, monkeys are deprived of having contact with adult monkeys for the first six months of life (Stevens et al., 2009). Instead, in the first month of their lives, monkeys are reared by animal caretakers in a nursery and subsequently housed with three to five peers. This paradigm is considered to reflect the experiences of children living in institutional care more closely than the “partial” or “total isolation” paradigms of Harlow, given that children growing up in institutions are typically deprived of a sensitive adult caregiver with whom they can develop a secure attachment, but they have opportunities to interact with peers.
Research has shown that although peer‐reared primates show attachment to their peers, their attachment is anxious (Stevens et al., 2009). This may be because peers may not be as effective as parents in regulating young monkeys’ fear and distress in the context of unfamiliar or distressing events. Consistent with this finding, peer‐rearing has been shown to have negative impact on primates’ ability to use a social companion to reduce stress as reflected by activation of the HPAA axis, a phenomenon referred to as “social buffering.” Specifically, in three‐year‐old rhesus monkeys, social partners were shown to buffer the stress response of the mother‐reared monkeys; however, the same level of buffering was not observed in the peer‐reared monkeys, suggesting that being deprived of early mother–infant relationship harms primates’ ability to benefit from social buffering (Winslow et al., 2003; for a review, see Hostinar et al., 2014).
Although peer‐reared monkeys showed normal physical and motor development, they developed into more anxious, impulsive, and aggressive individuals and often become more submissive, establishing themselves low in social hierarchy (Suomi, 2008). Their social play was observed to be less frequent and complex. They also showed increased preference for alcohol over nonalcoholic solutions (see Barr et al., 2004). Peer‐reared male monkeys have been shown to have increased levels of health problems in terms of frequency and prevalence compared to those reared by their mothers (Conti et al., 2012).
Peer‐rearing has been shown to lead to greater stress reactivity and disruptions in the hypothalamic‐pituitary adrenal (HPAA) functioning (for a review, Stevens et al., 2009). Specifically, peer‐reared monkeys show higher plasma cortisol (Shannon et al., 1998) and higher basal cortical levels, even after one and a half, and three years of normal social life (Feng et al., 2011). They experience altered neurotransmitter functioning such as lower levels of serotonin‐binding potential (Ichise et al., 2006) and metabolic alterations such as higher rates of whole‐brain glucose metabolism (Doudet et al., 1995).
The effects of peer deprivation in nonhuman primates.
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