Review
Series: Long-lasting Impact of Early-Life Stress and Adversity
Early Adversity and Critical Periods: Neurodevelopmental Consequences of Violating the Expectable Environment

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Highlights

  • Adversity might best be thought of as a violation of the expectable environment.

  • Adversity can take many forms, including exposure to biological and psychosocial hazards, which often coexist as complex exposures.

  • Many forms of early adversity are not time limited, making it difficult to tease apart the cumulative effects of adversity from the effects of early life adversity.

  • Exposure to various forms of adversity early in life is associated with alterations in brain development, which in turn is associated with psychological, behavioral, and physical health consequences.

  • Exposure to adversity during critical periods of development is more likely to lead to permanent rather than transient effects on the brain.

  • Parallel studies across humans and animal models of early adversity will prove essential to understanding how adversity becomes neurobiologically embedded.

It is now widely recognized that children exposed to adverse life events in the first years of life are at increased risk for a variety of neural, behavioral, and psychological sequelae. As we discuss in this paper, adverse events represent a violation of the expectable environment. If such violations occur during a critical period of brain development, the detrimental effects of early adversity are likely to be long lasting. Here we discuss the various ways adversity becomes neurobiologically embedded, and how the timing of such adversity plays an important role in determining outcomes. We conclude our paper by offering recommendations for how to elucidate the neural mechanisms responsible for the behavioral sequelae and how best to model the effects of early adversity.

Section snippets

A Conceptual Framework for Considering the Effects of Early Adversity on Brain Development

There is growing evidence that children exposed to adversity (see Glossary) early in life are at increased risk for atypical variations in brain development that in turn are associated with a variety of psychological, behavioral, and physical health sequelae [1., 2., 3.]. Adversity generally involves exposure to biological hazards (e.g., malnutrition, environmental toxins, chronic infection), psychological hazards (e.g., maltreatment, neighborhood or domestic violence), or both; and, although

What Do We Mean by ‘Adversity’?

Adversity has been used in a variety of ways. Some investigators have drawn analogies between early life stress and adversity [4., 5., 6.]. However, this can be misleading, as not all forms of adversity will be interpreted and/or encoded as stressful, depending on brain maturity and developmental history (e.g., an impoverished language environment, where a child is exposed to fewer words and less complex language, is likely a form of adversity but it is in and of itself not stressful and does

Adversity as a Violation of the Expectable Environment

For the purposes of this paper, we argue that adversity should be taken to reflect deviations in or disruptions of the expectable environment [22,23]; that is, experiences that are expected to occur (in order to confer survival and adaptation to the environment) either do not occur (e.g., lack of caregiving; lack of nutrition) or are atypical in some way (e.g., physical abuse). The reason an absence of an expected experience or the presence of an atypical experience matter can be attributed to

The Role of Critical Periods

Recently, Gabard-Durnam and McLaughlin [14] summarized several conceptual models that attempt to explain how adversity impacts neurodevelopment (Figure 2). These models emphasize different dimensions of adversity (e.g., timing, duration, type, number) or focus on how individual-level traits moderate the impact of an adverse experience [12,15., 16., 17., 18., 19.]. The conceptual models make assumptions not only about the most relevant features of environmental experience but also the underlying

Considering Critical Period Plasticity in the Context of Adversity

We wish to make several points to clarify the association between adversity and critical period plasticity. First, adversity is not itself an expectable experience that the brain prepares for. For example, the brain does not expect exposure to domestic violence. Adversity reflecting absent or impoverished specific expectable experiences clearly influences critical period inputs, but the adversity is not the expected substrate. Moreover, critical periods are inherently specific to particular

A High-Level Summary of the Effects of Adversity

We now consider the empirical evidence that early adversity can have enduring effects on human development. Countless studies have demonstrated an association between exposure to early, adverse life events and later maladaptive outcomes, with sequelae spanning a broad number of developmental domains. What follows is a cursory summary of some of the main findings.

Strategies to Parse the Effects of Adversity on Development

Given this robust literature linking early adversity with lasting impacts on development, a question that is currently receiving considerable attention empirically is how early adversity becomes neurobiologically embedded. Figure 4 complements the mechanisms highlighted in Figure 2 by illustrating a potential general model of biological embedding and sequelae across the lifespan. How may these conceptual models of biological embedding be translated into productive empirical strategies? At the

Concluding Remarks

Epidemiological studies dating back several decades advanced the idea that early adversity is associated with compromised neural and psychological outcomes. Recent work in neuroscience has begun to shed light on how a violation in experience-expected development during critical periods of brain development accounts for altered developmental outcomes. Not surprisingly, many questions remain unanswered (see Outstanding Questions). Moving forward, we advocate that this critical period approach

Acknowledgments

The writing of this paper was made possible by support to Charles A. Nelson from the Bill and Melinda Gates Foundation (OPP1111625), the National Institute of Mental Health (MH091363), and the Richard David Scott Chair in Pediatric Developmental Medicine Research, Boston Children’s Hospital; and to Laurel Gabard-Durnam from the University of Tokyo International Research Center for Neurointelligence.

Glossary

Adversity
a violation of the expectable environment that takes the form of biological hazards, psychosocial hazards, of complex exposures of both hazard types, with negative effects on development.
Biological embedding
the mechanisms through which environmental experiences impact neurobiology such that these experiences have enduring consequences on brain structure and function.
Biological hazard
adverse biological factors in the environment that have negative effects on development, such as

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