Elsevier

Psychoneuroendocrinology

Volume 32, Issue 7, August 2007, Pages 785-792
Psychoneuroendocrinology

Early life stress and novelty seeking behavior in adolescent monkeys

https://doi.org/10.1016/j.psyneuen.2007.05.008Get rights and content

Summary

Recent 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.

Introduction

Early exposure to severe forms of stress is a risk factor for the development of subsequent psychopathology (Agid et al., 1999; Heim et al., 2004). Interestingly, however, mildly stressful early experiences appear to promote the development of resilience (Fergus and Zimmerman, 2005; Rutter, 1993). People cope better with spousal loss, work-related stressors, and major accidents if they have previously experienced and coped with stress in childhood (Forest, 1991; Khoshaba and Maddi, 1999; Mortimer and Staff, 2004). Young monkeys exposed to intermittent stress (IS) and subsequently studied in unfamiliar situations likewise show fewer distress vocalizations and decreased maternal clinging compared to monkeys raised under no stress (NS) control conditions (Levine and Mody, 2003; Lyons et al., 1999; Parker et al., 2004, Parker et al., 2006). IS monkeys also more quickly initiate exploration and prefer to interact with novel vs. familiar objects compared to NS monkeys (Parker et al., 2004). These differences are of interest because engagement and mastery of novel situations is thought to foster adaptations that enhance self-regulation and resilience (Kashdan et al., 2004; Reio et al., 2006).

In our previous studies, differences between IS and NS monkeys in novelty seeking were confounded with differences in plasma levels of the stress hormone cortisol. Specifically, post-test cortisol levels were higher in NS compared to IS monkeys (Parker et al., 2004). The present study was designed to determine whether novelty seeking differences persist when adrenocortical responses to the test situation are minimized. This was accomplished by extensively acclimating monkeys to, and allowing monkeys to choose between, familiar and unfamiliar elements of the test. Novelty seeking behavior observed in this test situation was then compared to novelty seeking discerned in a previous study of the same monkeys (Parker et al., 2004) to examine cross-situational consistency in the expression of this behavior. We also investigated whether novelty seeking is associated with differences in cerebrospinal fluid (CSF) measures of various neurochemicals, as studies of humans and animals have linked novelty seeking to monoamines (Bardo et al., 1996; Gerra et al., 1999; Sara et al., 1995; Zuckerman, 1985) and stress-related neuropeptides (Kabbaj et al., 2000; Thorsell et al., 2006). We therefore examined relationships between novelty seeking and 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).

Section snippets

Subjects

Twenty squirrel monkeys (Samiri sciureus) of Guyanese origin born at the Stanford Research Animal Facility served as subjects. All monkeys received number tags worn on necklaces to facilitate easy identification. Subjects were reared in natal groups composed of three to four mother-infant pairs. Seasonal synchronous breeding facilitated generation of an age-matched study cohort, and all infants were born within a 2-month period. Group composition was determined by infant birth dates to minimize

Rearing differences in novelty seeking behavior

All IS monkeys (11 of 11) and all but one of the NS monkeys (8 of 9) approached the threshold of the novel test box and peered into it during testing (χ2=1.287, df=19, p=0.257). Monkeys from both of the rearing conditions were therefore aware of the test box, but IS monkeys contacted the box threshold faster (F1,18=7.425, p=0.014), were in more frequent contact with the box threshold (F1,18=12.876, p=0.002), and spent more time on the box threshold (F1,18=5.584, p=0.030) compared to NS monkeys.

Discussion

Results from this study confirm that IS monkeys engage in more novelty seeking behavior than NS monkeys. Differences in novelty seeking occurred in the absence of adrenocortical activation and do not appear to reflect stress-related anxiety. 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 findings suggest that mildly stressful early experiences

Role of funding source

The funding sources had no role in the collection, analysis and interpretation of data; in the writing of the report; or in the decision to submit the manuscript for publication.

Conflict of interest

All authors declare that no conflict of interest, financial or otherwise, exists with regard to this research.

Acknowledgements

Dr. Parker was supported by MH66537 from the National Institute of Mental Health, Bethesda, MD and a Stanford University School of Medicine Dean's Fellowship. This research was supported by MH47573 and MH50604 from the National Institute of Mental Health; DA16902 from the National Institute on Drug Abuse, Bethesda, MD; and the Nancy Pritzker Network, New York, NY. We gratefully acknowledge Dr. James Ritchie for technical advice on the CRF assay, Dr. Jamie Zeitzer for assistance with blood

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