Indeed, Bowlby’s attachment theory, which was built off this foundation of research, is still deemed to be an important conceptual framework for understanding the role of early social relationships and their absence in both animal and human research.
Nonhuman Primate Models
Why are Nonhuman Primate Models Useful?
Nonhuman primates are the evolutionarily closest animals to humans (Kumar & Hedges, 1998) and, therefore, provide important models to understand the potential effects of deprivations in social experiences on humans. Rhesus monkeys, perhaps the most commonly used nonhuman primates in research, share similarities with humans (Phillips et al., 2014). They share approximately 95% of their genes with humans, and the structure and functional organization of their brains are highly similar to human brains (Stevens et al., 2009). For example, rhesus monkeys’ neocortex constitutes 72% of the brain volume, whereas humans’ neocortex constitutes 80% of the brain volume (Passingham, 2009). In vast contrast, rats’ neocortex comprises only 28% of the rat brain. Consistent with the similarities in neural architecture, primates are also capable of more advanced cognitive skills such as inhibitory control and delay of gratification, and therefore, are good models for examining the effects of early experiences on the development of higher‐level cognition (see Phillips et al., 2014). Similar to humans, nonhuman primates have extended life spans with distinct developmental periods such as infancy, childhood, and adolescence. They spend their early months in close proximity with their caregivers developing an attachment relationship and, then, become gradually more independent from caregivers over time, spending more of their time with peers.
Their social and emotional intelligence also make them good models to understand psychological processes (Phillips et al., 2014). For example, several nonhuman primates including rhesus monkeys and chimpanzees demonstrate complex communication patterns, live in social groups, and demonstrate social learning ability of complex behaviors such washing food before consumption (Stevens et al., 2009). They have the ability to recognize themselves as well as others (see Phillips et al., 2014). Specifically, they are able to discriminate between familiar and unfamiliar faces, recognize individuals’ faces from photos, and understand other conspecifics’ facial expressions (see Phillips et al., 2014).
Nonhuman primates possess relatively stable temperamental and personality dimensions that are comparable to the dimensions studied in humans (Capitanio & Widaman, 2005). For example, chimpanzees have relatively stable traits such as sociability, positive affect, anxiety, and equitability (see Phillips et al., 2014). Likewise, rhesus monkeys’ temperament during infancy has been associated with both the quality (i.e., reciprocated relationships) and quantity (i.e., how much time they spend with others) of their social relationships during juvenile years (Weinstein & Capitanio, 2008). These similarities allow researchers to examine how early experiences such as social deprivation 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
