Review
Evolutionary functions of early social modulation of hypothalamic-pituitary-adrenal axis development in humans

https://doi.org/10.1016/j.neubiorev.2011.01.005Get rights and content

Abstract

The hypothalamic-pituitary-adrenal axis (HPAA) is highly responsive to social challenges. Because stress hormones can have negative developmental and health consequences, this presents an evolutionary paradox: Why would natural selection have favored mechanisms that elevate stress hormone levels in response to psychosocial stimuli? Here we review the hypothesis that large brains, an extended childhood and intensive family care in humans are adaptations resulting from selective forces exerted by the increasingly complex and dynamic social and cultural environment that co-evolved with these traits. Variations in the modulation of stress responses mediated by specific HPAA characteristics (e.g., baseline cortisol levels, and changes in cortisol levels in response to challenges) are viewed as phenotypically plastic, ontogenetic responses to specific environmental signals. From this perspective, we discuss relations between physiological stress responses and life history trajectories, particularly the development of social competencies. We present brief summaries of data on hormones, indicators of morbidity and social environments from our long-term, naturalistic studies in both Guatemala and Dominica. Results indicate that difficult family environments and traumatic social events are associated with temporal elevations of cortisol, suppressed reproductive functioning and elevated morbidity. The long-term effects of traumatic early experiences on cortisol profiles are complex and indicate domain-specific effects, with normal recovery from physical stressors, but some heightened response to negative-affect social challenges. We consider these results to be consistent with the hypothesis that developmental programming of the HPAA and other neuroendocrine systems associated with stress responses may facilitate cognitive targeting of salient social challenges in specific environments.

Section snippets

Evolutionary paradox of psychosocial stress

Psychosocial challenges reliably stimulate the hypothalamic-pituitary-adrenal axis (HPAA) in humans and many other mammals (Hennessey et al., 2009, Yim et al., 2010). Given the apparent short- and long-term costs of HPAA activation to physical and mental health (Cohen, 2004, Kiecolt-Glaser et al., 2010, Shonkoff et al., 2009), this presents an evolutionary paradox: Why do social interactions and relationships affect HPAA responses? Currently no satisfactory explanations exist for why natural

Physiological mechanisms, developmental plasticity and adaptive function

Most studies of social modulation of early HPAA development have been based on clinical, epidemiological and experimental (primarily nonhuman animal model) research paradigms. Tremendous advances have been made in understanding the physiological, neurobiological and genetic mechanisms that underpin stress responses (de Kloet et al., 2005b, Joëls and Baram, 2009, Lupien et al., 2009, McEwen, 2007, Sapolsky et al., 2000, Weaver et al., 2004). Explanations for early social modulation of HPAA

Stress in the wild: HPAA responses in natural, everyday context

“What is missing are long term prospective studies that track the nature and timing of early stress exposure and the linkages to children's later stress exposure, HPA functioning, and behaviors” (Essex et al., 2002, p. 777).

Investigating relations among HPAA responses, neural remodeling and cognitive adaptations to the social environment is not a simple or easy task (e.g., Pine et al., 2001). While cortisol can affect cognitive functioning and emotional states, cognitive processing and

Concluding remarks

Returning to the paradox of why natural selection favored sensitivity of stress response to social stimuli in the human child, several points emerge. Human childhood is a life history stage that appears necessary and useful for acquiring the information and practice to build and refine mental algorithms critical for negotiating the social coalitions that are key to success in our species. Mastering the social environment presents special challenges for the human child. Results from the

Acknowledgements

Our research efforts have primarily been funded by NSF BCS-SBE-0640442, SBR-0136023, SBR-9205373, & BNS-8920569 (MVF, MPM, DP), and Simon Fraser University – President's Research Start Up Grant (PAN) and CIHR Operating Grant # 106705. We thank Dr. Katrina Salvante for her assistance with figure 2 and Dr. Robert Walker for help with figure 4.

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