Long‐term effects of differential early rearing in rhesus macaques: Behavioral reactivity in adulthood

Abstract

Adverse early experiences are associated with a range of deleterious health outcomes in humans, including higher risk for affective disorders. Studies using a long-standing model of nonhuman primate model of early adversity have demonstrated that nursery-reared monkeys exhibit alterations in multiple aspects of biobehavioral development; however, few studies have evaluated the persistence of socioaffective behavioral changes through adulthood. We evaluated the effects of early rearing experience on adult animals’ response to a well-validated assessment of anxiety-like behavior, the Human Intruder Paradigm (HIP). We tested twenty-two rhesus monkeys who were either nursery-reared (NR) or reared with their mothers (mother-reared; MR). NR monkeys were inhibited in their behavior compared to MR monkeys, with reduced locomotion and exploratory behaviors. NR animals showed a marginal increase in freezing. Together these findings demonstrate that the consequences of differential infant rearing experience on socioaffective behavior persist into adulthood, with evidence of greater inhibition in NR monkeys.

Disruptions in serotonergic regulation of cortical glutamate release in primate insular cortex in response to chronic ethanol and nursery rearing

“…Nursery-rearing in nonhuman primates has been shown to result in behavioral and neurochemical changes later in life consistent with affective disorders, and these animals have been reported to consume greater quantities of ethanol relative to MR animals (Harlow et al, 1959; Harlow et al, 1965; Harlow & Suomi, 1974; Seay & Harlow, 1965; Suomi, 1997; Shannon et al, 1998; Sanchez et al, 2001; Machado & Bachevalier, 2003; Cirulli et al, 2009; Higley et al, 1991). Consistent with this, a parallel study using the mother-reared (MR) and nursery-reared (NR) ethanol-naïve monkeys that were also used in the current study reported altered socioaffective behavior in NR monkeys compared to MR monkeys (Corcoran et al, 2011). This model thus provides a unique resource to understand neurobiological changes similar to those that may occur in human children exposed to early-life stress and how these changes may contribute to the development of addictive behaviors later in life.…”

Acute oxytocin improves memory and gaze following in male but not female nursery-reared infant macaques

“…Finally, the present study focused on infants who were raised by human caretakers. This unique rearing may have impacted infants’ early OT systems (Corcoran et al 2012; Winslow et al 2003); studies in mother-reared infants are necessary to determine the generalizability of our results. Nonetheless, the present results extend previous findings of positive social effects of OT in infant monkeys (Simpson et al 2014), suggesting OT effects also appear in more cognitive tasks.…”

Early-life social adversity and developmental processes in nonhuman primates

“…Macaques reared in sub-optimal mother-only conditions show higher fear and anxiety responses to a stress-inducing challenge than those from rearing conditions in which multiple adults and peers are present [1]. These affective responses, also characterized by pronounced behavioral inhibition, in SOR-exposed macaques persist well into adulthood [4]. Some behavioral effects of ELSA may not be long lasting, as macaques that experienced STS as infants displayed normative behavioral reactivity when placed in short-term social isolation as adults [5].…”