Early childhood stress exposure, reward pathways, and adult decision making

Abstract

Individuals who have experienced chronic and high levels of stress during their childhoods are at increased risk for a wide range of behavioral problems, yet the neurobiological mechanisms underlying this association are poorly understood. We measured the life circumstances of a community sample of school-aged children and then followed these children for a decade. Those from the highest and lowest quintiles of childhood stress exposure were invited to return to our laboratory as young adults, at which time we reassessed their life circumstances, acquired fMRI data during a reward-processing task, and tested their judgment and decision making. Individuals who experienced high levels of early life stress showed lower levels of brain activation when processing cues signaling potential loss and increased responsivity when actually experiencing losses. Specifically, those with high childhood stress had reduced activation in the posterior cingulate/precuneus, middle temporal gyrus, and superior occipital cortex during the anticipation of potential rewards; reduced activation in putamen and insula during the anticipation of potential losses; and increased left inferior frontal gyrus activation when experiencing an actual loss. These patterns of brain activity were associated with both laboratory and real-world measures of individuals' risk taking in adulthood. Importantly, these effects were predicated only by childhood stress exposure and not by current levels of life stress.

Keywords: childhood development; decision making; early life stress; reward; social behavior.

Conflict of interest statement

The authors declare no conflict of interest.

Copyright © 2017 the Author(s). Published by PNAS.

Figures

Fig. 1.

Schematic of the MID task used in this study. Participants were presented with a cue indicating the amount of potential monetary gain or loss. A triangle (“TARGET”) briefly appeared on the screen, and the participant had to press a button while the triangle was on the screen to win or avoid losing money. Pressing the button too early or too late resulted in no win or a loss. Feedback was then provided to indicate success or failure on that trial.

Fig. 2.

Brain areas where the difference between the anticipation of potential large rewards (+$5) vs. no rewards (+$0) is significantly correlated with early life stress. Blue regions indicate areas where the brain activation during the anticipation of potential rewards vs. no rewards is negatively correlated with early life stress. That is, the participants with higher early life stress showed lower activation in the precuneus, middle temporal gyrus, and cerebellum during the anticipation of potential rewards (P < 0.05).

Fig. 3.

Brain areas where the difference between the anticipation of potential large losses (−$5) vs. no loss (−$0) is significantly correlated with early life stress. Blue regions indicate areas where the brain activation during the anticipation of potential losses vs. no loss is negatively related to early life stress. That is, subjects with higher early life stress showed lower activation in the insula and putamen during the anticipation of potential losses (P < 0.01).

Fig. 4.

Brain areas where differences in the response to missing the target on a loss vs. no-loss trial (i.e., response to losing money) is correlated with early life stress. Yellow/orange regions show brain areas where the activation during the response to loss vs. no-loss trials is positively correlated with early life stress. Significantly greater activation was observed in the putamen and inferior frontal gyrus in subjects with higher early life stress.

Fig. 5.

Individual differences in risky behaviors, measured from the Youth Risk Behavior Survey, are correlated with measures of early life stress (assessed using the YLSI; P < 0.0003). This effect held even after controlling for current life stress (assessed using the LSI; P < 0.05).

Fig. 6.

Across participants, an index of risky behaviors (measured from the Youth Risk Behavior Survey) is significantly correlated with the activation of the putamen during the anticipation of potential loss in the MID task (A), but not with the activation in the left inferior frontal gyrus during the response to the loss (B).