The Impact of Developmental Timing for Stress and Recovery

Dylan G Gee, B J Casey, Dylan G Gee, B J Casey

Abstract

Stress can have lasting effects on the brain and behavior. Delineating the impact of stress on the developing brain is fundamental for understanding mechanisms through which stress induces persistent effects on behavior that can lead to psychopathology. The growing field of translational developmental neuroscience has revealed a significant role of the timing of stress on risk, resilience, and neuroplasticity. Studies of stress across species have provided essential insight into the mechanisms by which the brain changes and the timing of those changes on outcome. In this article, we review the neurobiological effects of stress and propose a model by which sensitive periods of neural development interact with stressful life events to affect plasticity and the effects of stress on functional outcomes. We then highlight how early-life stress can alter the course of brain development. Finally, we examine mechanisms of buffering against early-life stress that may promote resilience and positive outcomes. The findings are discussed in the context of implications for early identification of risk and resilience factors and development of novel interventions that target the biological state of the developing brain to ultimately ameliorate the adverse consequences of stress during childhood and adolescence.

Keywords: amygdala; development; early-life stress; neuroplasticity; prefrontal cortex; resilience; sensitive period.

Figures

Fig. 1
Fig. 1
Model of sensitive periods of brain development. Periods of rapid and substantial changes in brain development, such as the first three years of life and adolescence (shaded in gray), may provide the most opportunity for adaptive behavioral changes. These sensitive periods of neural development may also render the developing brain most vulnerable to the effects of stress. Figure adapted with permission from Lee et al., 2014 (Copyright 2014 AAAS).
Fig. 2
Fig. 2
Mature frontoamygdala functional connectivity following maternal deprivation. Left) A group by emotion interaction was observed in the mPFC (p Proceedings of the National Academy of Sciences of the United States of America).
Fig. 3
Fig. 3
Greater amygdala activity in humans and mice following early-life stress. (A) Human participants were instructed to detect frequently presented neutral targets embedded among rare threat non-target cues. Mice were trained where to obtain sweetened milk in their home cage for 3 consecutive days and then latency to approach the milk was measured in the home cage on the 4th day, and in an odorless, brightly lit novel cage on the 5th day. (B) Stressed preadolescent humans and mice take longer than their standard-reared counterparts to approach targets in the context of potential threat. (C) Amygdala activity in response to threat was greater in stressed preadolescent humans and mice than their standard-reared counterparts. Error bars = +/− 1 SEM. Data are reproduced with permission from Malter Cohen et al., 2013a, Malter Cohen et al., 2013b (Copyright 2013 Proceedings of the National Academy of Sciences of the United States of America).
Fig. 4
Fig. 4
c-Fos activity by group and age. (A) The density of c-Fos protein in the amygdala following exposure to the threatening context (i.e. novel cage) was elevated in stressed mice across development relative to nonstressed animals. (B) The density of c-Fos protein in the infralimbic PFC increases with age regardless of stress history. Error bars = +/− 1 SEM; *p Proceedings of the National Academy of Sciences of the United States of America).
Fig. 5
Fig. 5
Maternal buffering of amygdala reactivity and mature-like connectivity in childhood. (A) Presence of the maternal stimulus phasically buffered right amygdala reactivity in children but not adolescents (p = 0.049). Specifically, children showed lower activation of the right amygdala to their mother compared with a stranger (i.e., the mother of another youth). (B) The psychophysiological interaction analysis of amygdala–mPFC functional connectivity revealed an interaction between age group and the maternal stimulus manipulation (p = 0.034). Specifically, adolescents showed a mature pattern of inverse amygdala–mPFC functional connectivity to both their mother and the stranger. In contrast, children exhibited a mature-like, inverse pattern of functional connectivity to their mother (p = 0.019). However, functional connectivity to the stranger did not differ from implicit baseline in children, suggesting that the phasic presence of the maternal stimulus may induce a more mature-like pattern of amygdala–prefrontal interaction in childhood. *p Psychological Science).
Fig. 6
Fig. 6
Stress effects on human PFC function (Bottom) are consistent with those observed in a rodent model of chronic stress (Top). (A) Chronic stress disrupted dorsolateral PFC functional connectivity in human participants (t = 5.74, p The Journal of Neuroscience). Data from the human study are reproduced with permission from Liston et al., 2009 (Copyright 2009 Proceedings of the National Academy of Sciences of the United States of America).

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Source: PubMed

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