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Early adversity, stress, and neurobehavioral development

In 1956, Seymour Levine and colleagues (Levine, Chevalier, & Korchin, 1956) took a group of infant rats and subjected them to mild shocks every day. They then compared the pups’ ability to learn in adulthood to two groups: one group that was handled but not shocked, and one group that was not handled nor were their nests disturbed. This was one of the first experimental studies of early adversity and the results were shocking (no pun intended). The group that was impaired in learning was the group who had not been handled or shocked. The handled-shocked and the handled-only group did equally well on every measure. Thus was born the research area known as infantile stimulation. Infant stimulation was shown to alter behavior into adulthood, to be most effective during a sensitive period in the first two weeks of life, to reduce fearfulness, increase stress resistance, and delay immune senescence. When President Johnson declared a war on poverty and had Sargent Shriver convene the task force that created Head Start, the work on infantile stimulation, among others, supported the idea that infancy and early childhood was a critical period for providing stimulation. The fact that electric shocks produced positive effects on development seems to fly in the face of our current attempts to explain why early adversity has long-term negative impacts on human development. Perhaps the problem is that rats and mice are not good models of humans. In this case, that is unlikely. Recall the rodent infantile stimulation work was paralleled by the cultural anthropology of Landauer and Whiting (1964) who showed more robust physical growth in cultures that exposed their infants to various forms of stress from circumcision to cold baths. There is a great deal of excellent food for thought in that early literature as we attempt to understand how early adversity “gets under the skin” to influence long-term outcomes in human development. Some of the themes and findings from that early work reappear in the pages of this special issue, although frequently not attributed to these early origins. For example, the early literature identified stimulation as having a U-shape function in relation to adult outcomes: too little and too much was associated with poorer outcomes (Denenberg, 1964). We have rediscovered this in the theorizing of Boyce and Ellis (2005) who argue that too little and too much adversity are both associated with higher stress reactivity, while a moderate amount of adversity within the child’s ability to cope is associated with reduced, but not hypoactive reactivity. An example of issues that the early rodent work highlighted that we should revisit but have not is the possibility that noxious stimulation has opposing effects at different points in development. Thus, the same levels of shock that in preweaning rat pups results in less fearful behavior, when delivered to postweaning animals impairs functioning (Denenberg, 1964). That early work is reminiscent of current work by Regina Sullivan showing that in infant rat pups pairing a novel odor with shock results in a preference for and approach to the odor if the dam is present and an aversion when she is absent, while in older animals only an aversion is observed (see review Hostinar, Sullivan, & Gunnar, 2014). While this might seem unlikely in humans, Nim Tottenham and colleagues (Tottenham, Shapiro, Flannery, Caldera, & Sullivan, 2019) have recently shown something quite similar in preschool-age children. After being conditioned to identify one stimulus with a noxious event, preschool-aged children actually showed a preference for that stimulus when the parent was present, but avoided it when the parent was not present. These data indicate that the attachment figure moderates how aversive stimuli impact the young child, but perhaps not the older child, as will be discussed. Another theme in the early work was that the effects of infantile stimulation were likely mediated by what it did to parental care. Specifically, when the pup was either handled or shocked it was returned to the dam in an agitated state. That elicited heightened nurturing stimulation (licking and grooming) by the dam which in reality was the critical feature of the infant’s experience (Smotherman & Bell, 1980). While sometimes controversial (Denenberg, 1999), it is largely accepted that stimuli as disparate as handling and shock produce similar outcomes because they both result in heightened maternal care. Similarly, the early adversity literature in human development converges on parental care as the central protective factor and the process that, when it fails the child, becomes the main conduit for adversity to impact the child’s development. These themes from the early animal literature have strong resonance in our current work on early adversity, stress, neurobehavioral development, and resilience. In what follows I will outline many of the current issues with which the field is grappling and point to papers in this special issue that reflect these issues.