Early adverse experience increases emotional reactivity in juvenile rhesus macaques: Relation to amygdala volume

Abstract

This study investigated the impact of infant maltreatment on juvenile rhesus monkeys’ behavioral reactivity to novel stimuli and its associations with amygdala volume. Behavioral reactivity to novel stimuli of varying threat intensity was measured using Approach/Avoidance (AA) and Human Intruder (HI) tasks. In vivo magnetic resonance imaging (MRI) was used to measure amygdala volume. Interestingly, group behavioral differences were context-dependent. When exposed to a human intruder, maltreated subjects displayed more anxious behaviors than controls; however, when presented with fear-evoking objects, maltreated animals exhibited increased aggression and a shorter latency to inspect the objects. Finally, under testing conditions with the lowest levels of threat (neutral novel objects) maltreated animals also showed shorter latencies to inspect objects, and reduced avoidance and increased exploration compared to controls. This suggests alterations in threat assessment and less behavioral inhibition in animals with early adverse experience compared to controls. Some of these behavioral responses were associated with amygdala volume, which was positively correlated with abuse rates received during infancy, particularly reflecting a relationship with exploration, consistent with previous studies.

Early-life social adversity and developmental processes in nonhuman primates

“…Macaques exposed to SOR showed lower levels of distress during a developmental assessment compared to control animals [10]. Squirrel monkeys exposed to STS and macaques that experienced early life abuse showed increased exploratory behavior in the context of novel objects and environments [2,11,12]. These findings suggest that some benefits may derive from ELSA, such as increased resistance to the stress of novel nonsocial situations.…”

“…Abused infant macaques display deficits in emotional expression such as the use of inappropriate vocalizations in response to contact and non-contact aggression [13]. Abused infants also exhibit high rates of distress vocalizations and anxiety-related behavior during normal social interactions, and in response to stressors and high-fear stimuli (animated toy accompanied by sounds) [11,14]. However, abused macaques show reduced anxiety-related behavior when exposed to low-fear or neutral stimuli (roll of tape) [11].…”

“…Abused infants also exhibit high rates of distress vocalizations and anxiety-related behavior during normal social interactions, and in response to stressors and high-fear stimuli (animated toy accompanied by sounds) [11,14]. However, abused macaques show reduced anxiety-related behavior when exposed to low-fear or neutral stimuli (roll of tape) [11]. This differential response to low- and high-fear stimuli suggests that macaques that have experienced SOR have an altered system for threat assessment, with an increased threshold required to elicit a behavioral response relative to infants with normal developmental environments.…”

“…ELSA in macaques is associated with significant structural changes in the brain, including larger volumes of the anterior cingulate cortex (ACC) and dorsomedial prefrontal cortex (dmPFC) [41], reduced hippocampal and temporal gyri volume [43], and larger amygdala volume [11]. ELSA also selectively alters regional metabolic activity in the brain of macaques.…”

When mothering goes awry: Challenges and opportunities for utilizing evidence across rodent, nonhuman primate and human studies to better define the biological consequences of negative early caregiving

“…For example, recent NHP neuroimaging studies have demonstrated a positive correlation between abuse rates experienced during infancy and amygdala volume, as well as reduced white matter integrity in tracts important for behavioral and emotional regulation that were also associated with elevated levels of cortisol in abused infants (Howell et al, 2014, 2013). These findings parallel findings reported in maltreated humans and children exposed to extreme psychosocial deprivation as a consequence of institutional care.…”