The Stress Acceleration Hypothesis: effects of early-life adversity on emotion circuits and behavior

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Highlights

  • Early caregiving adversity is associated with poor mental health outcomes.

  • Across species, adversity accelerates the developmental trajectory of emotion circuits.

  • Accelerated development may reflect an adaptive strategy for low parental care contexts.

  • Changes to the pace of development may change the nature of mature phenotypes.

  • A model is proposed that provides a neurobiological mechanism by which early experiences lead to changes in emotional phenotypes.

The importance of early experiences for mental health across the lifespan is well recognized. In particular, there is a strong association between adverse caregiving experiences and mental illness. However, relative to studies assessing outcomes in adults, there are far fewer studies assessing the earlier emerging manifestations of caregiving adversity during development. This lack of developmental research limits an understanding of the mechanisms that link adversity with mental illness. Adoption of a developmental approach to research in this field will yield greater insights into the factors that tie adversity to poor emotion function across a lifespan. In this review, we focus on recent findings that have used a developmental approach in the examination of mental health and early adversity. These studies are notable in that, across numerous species, they converge on the idea that early adversity leads to accelerated maturation of emotion circuits in the brain and in the behaviors supported by these regions. We propose that these ‘stress acceleration’ effects are evidence of early system adaptation.

Introduction

It has long been recognized that early experiences establish the foundation for life long mental health. Arguably the most important of these early experiences is the ongoing parent–child relationship. Indeed, being born into and brought up within a stable home can be a powerful factor contributing to mental wellbeing [(e.g., 1)]. However, the opposite is also true; dysfunctional early caregiving (such as neglect, parental mental illness, and familial violence) is strongly associated with mental illness, accounting for up to 45% of child-onset, and 32% of adult-onset mental health disorders (including anxiety, mood and psychotic disorders) [2, 3]. While the relationship between early experiences of adversity and mental illness is often observed, the mechanisms linking these experiences are not well articulated. Hence, understanding how early experiences get ‘under the skin’ to influence an individual across his/her lifespan is one of the central goals of research in the affective neurosciences.

One predominant perspective on the link between early adversity and mental illness is that such early experiences impair brain function, as children with histories of adversity reliably perform more poorly on tests of language and cognition [4, 5, 6]. However, numerous theories now predict that, rather than leading to general deficits or delays, adversity may in fact lead to a reprioritization of developmental strategy away from a neotenous state (which favors a slow developmental pace and prolonged childhood [7]) and toward more adult-like functioning within fear/stress-related domains [8••, 9, 10, 11, 12, 13]. For example, many theories operating within an evolutionary biology framework (including Life History Theory, Psychosocial Acceleration Hypothesis, Child Development Theory, and the Adaptive Calibration Model) posit that our evolutionary history selected for plasticity in developmental trajectories, such that early experiences could program the length of childhood and the age of pubertal transition [9, 10, 12, 13]. Specifically, these theories suggest that slower developmental strategies would be advantageous in conditions of low stress, allowing the individual to absorb information from the social and family environment early in life that may increase survival and parenting skills before transitioning into the reproductive stage of development. By contrast, faster developmental strategies allowing for earlier reproduction are proposed to increase reproductive success and fitness in contexts of adversity where long-term survival is uncertain. Indeed, in support of these theories, there is considerable evidence demonstrating that the age of pubertal maturation is negatively associated with levels of stress in the early environment (e.g., reviewed in [9]).

The frameworks discussed above are persuasive in their description of accelerated patterns of development as adaptations to contexts of early adversity (as opposed to traditional views that stress diminishes functionality). However, the mechanisms behind how such altered trajectories are related to the higher rates of mental illness seen in adversity-exposed populations remain elusive. The fact that caregiving adversity is associated with both accelerated development of emotion behavior/neurobiology, as well as increased risk for mental illness compellingly suggests that the two outcomes may be mechanistically related. Our goal in the current paper is to provide a neurobiological framework (the Stress Acceleration Hypothesis) within which to conceptualize such stress-induced accelerations, particularly those that occur within stress and fear systems. Using this framework, we then consider whether the early changes in trajectories of affective neurocircuitry are associated with later emergences of mental health disorders. Although these links have yet to be established within a single study over developmental time, the theory attempts to provide a mechanistic link between early adversity and mental illness (e.g., depression, anxiety) that is established in the literature [2]. We begin the paper by reviewing behavioral, then neural, studies of stress acceleration effects on fear systems, before putting forward the Stress Acceleration Hypothesis and discussing how accelerated outcomes may be mechanistically linked to mental health/illness.

Section snippets

Behavioral studies demonstrating stress acceleration effects

While the development of emotional learning and emotion regulation has been investigated for some time in rodent studies (e.g., [14]), there are far fewer examples of research explicitly investigating the interaction between rearing environments and the maturation of emotion learning in any species. Interestingly, those studies that have focused on that interaction report that rearing adversity has significant consequences for two forms of emotion learning with clear clinical implications  fear

Neural studies demonstrating stress acceleration effects

Some of the first studies to investigate the effect of early adversity on the neural circuits involved in fear learning and extinction focused on the amygdala. Critically, across many species it was shown that rearing adversity had dramatic effects of amygdala structure and function that appear to indicate accelerated development. In terms of amygdala function, previous studies have shown that stress leads to precocious involvement of the amygdala in fear learning. For example, the transition

The stress acceleration hypothesis

The studies discussed above converge on the finding that, across species, early life caregiving stress prematurely activates and accelerates the maturation of various neural structures, functional profiles, and molecular compositions, in brain regions important for emotion expression, and associative learning and memory. We propose that accelerated phenotypes emerge because stress experienced early in life may prematurely activate the core circuitry of emotional learning and reactivity [11].

Conclusion

The studies discussed in this review strongly suggest that accelerated development of emotion behaviors and circuits is a core outcome following the experience of rearing adversity. We suggest that such accelerated development may have implications for the integrity of emotion circuits and emotion regulation later in life. It remains possible that these neural adaptations are in fact indicators of longer-term mental health resilience  a solid understanding of these adaptations continues to be

Conflict of interest

The authors declare that they have no conflicts of interest to report.

Acknowledgments

This research was supported by National Institute of Mental Health Grant R01MH091864 (to N. Tottenham), by the Dana Foundation (to N. Tottenham), and National Health and Medical Research Council Early Career Fellowship 1091571 (to B. Callaghan).

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