Early life stress and novelty seeking behavior in adolescent monkeys

Abstract

SUMMARYRecent evidence suggests that early exposure to mild stress promotes the development of novelty seeking behavior. Here we test this hypothesis in squirrel monkeys and investigate whether novelty seeking behavior is associated with differences in cerebrospinal fluid (CSF) levels of the serotonin metabolite 5-hydroxyindoleacetic acid (5HIAA), the dopamine metabolite homovanillic acid (HVA), the norepinephrine metabolite 3-methoxy-4-hydroxyphenylethylene glycol (MHPG), and the neuropeptide corticotrophin-releasing factor (CRF). Monkeys were randomized early in life to either mild intermittent stress (IS) or no stress (NS) conditions, and subsequently presented with opportunities to interact with a familiar or novel object in a test box that was connected to each monkey's home cage. To further minimize the potentially stressful nature of the test situation, monkeys were acclimated to the test procedures prior to study initiation. Post-test plasma levels of cortisol in IS and NS monkeys did not differ significantly from baseline levels measured in undisturbed conditions. During testing, more IS than NS monkeys voluntarily left the home cage, and IS monkeys spent more time in the test box compared to NS monkeys. More IS than NS monkeys engaged in object exploration in the test box, and IS monkeys preferred to interact with the novel vs. familiar object. Novelty seeking was not associated with differences in 5HIAA, HVA, MHPG, or CRF, but correlated with differences in object exploration observed in a different test situation at an earlier age. These trait-like differences in novelty seeking appear to reflect mild early stress-induced adaptations that enhance curiosity and resilience.

Prefrontal Plasticity and Stress Inoculation-Induced Resilience

“…Increased ventromedial prefrontal cortical volumes reflect surface area expansion and coincide with increased white matter myelination inferred from neuroimaging. In published studies of the same monkeys, we previously reported that intermittent separations diminish subsequent stress-levels of cortisol, increase exploration of novel situations, and enhance prefrontal-dependent cognitive control of behavior [15,17,18] . Taken together, these findings suggest a role for prefrontal neuroadaptations in arousal regulation and resilience.…”

“…Mothers were then permanently removed and their offspring were housed with peers. Cognitive control of behavior was assessed at 1.5 years of age [18] and exploratory behavior was examined at 2.5 years of age [17] . Puberty occurs at 2-3 years of age and the average maximum life span is ϳ 21 years.…”

“…Initially, brief intermittent separations studied in controlled experimental conditions elicit distress peep calls and increase plasma levels of cortisol with partial habituation of these measures of arousal observed over repeated social separations [11,12] . Later in life, monkeys exposed to intermittent separations show fewer behavioral indications of anxiety, increased exploration of novel situations, and diminished stress levels of cortisol compared to agematched monkeys not exposed to prior separations [13][14][15][16][17] . These behavioral and hormonal outcomes reflect a nonspecific form of stress inoculation [15] as exposure to one type of early life stress enhances subsequent arousal regulation and resilience in coping with different stressors encountered later in life.…”

Stress inoculation‐induced indications of resilience in monkeys

“…This was accomplished by monitoring exploration of novel and familiar objects presented in a stress-free condition (Parker et al, 2007). Briefly, a familiar and a novel object were each secured to the back wall of a test compartment.…”

“…However, more stress inoculated than noninoculated monkeys entered the compartment, and stress inoculated monkeys entered faster, with greater frequency, and spent more time inside the test compartment compared to noninoculated monkeys (Figure 3). In addition, more stress-inoculated than noninoculated monkeys explored the objects inside the compartment, and stress-inoculated monkeys preferred to explore the novel compared to the familiar object (Parker et al, 2007).…”