Striatum-medial prefrontal cortex connectivity predicts developmental changes in reinforcement learning

Abstract

During development, children improve in learning from feedback to adapt their behavior. However, it is still unclear which neural mechanisms might underlie these developmental changes. In the current study, we used a reinforcement learning model to investigate neurodevelopmental changes in the representation and processing of learning signals. Sixty-seven healthy volunteers between ages 8 and 22 (children: 8-11 years, adolescents: 13-16 years, and adults: 18-22 years) performed a probabilistic learning task while in a magnetic resonance imaging scanner. The behavioral data demonstrated age differences in learning parameters with a stronger impact of negative feedback on expected value in children. Imaging data revealed that the neural representation of prediction errors was similar across age groups, but functional connectivity between the ventral striatum and the medial prefrontal cortex changed as a function of age. Furthermore, the connectivity strength predicted the tendency to alter expectations after receiving negative feedback. These findings suggest that the underlying mechanisms of developmental changes in learning are not related to differences in the neural representation of learning signals per se but rather in how learning signals are used to guide behavior and expectations.

Figure 1.

(A) Participants chose one stimulus by pressing the left or right button and received positive or negative feedback according to probabilistic rules. Two pairs of stimuli were presented to the participants: (1) the AB pair with 80% positive feedback for A and 20% for B and (2) the CD pair with 70% positive feedback for Cand 30% for D. (B) Estimated model fits per age group. (C) Estimated learning rates for positive and negative feedback per age group. Error bars represent standard errors in all graphs.

Figure 2.

(A) Regions in the mPFC, ventral striatum, and parahippocampal gyrus in which BOLD signal was significantly correlated with prediction errors. Thresholded at P < 0.05, FWE, k > 10. (B) Parameter estimates of the prediction errors per age group in the functionally defined ROIs for the mPFC, ventral striatum, and parahippocampal gyrus.

Figure 3.

(A) Regions that showed increased functional connectivity with the striatal seed region after positive compared with negative feedback. Thresholded at P < 0.05, FWE, k > 10. (B) Region in the mPFC that revealed age-related changes in functional connectivity with the striatal seed region. Thresholded at P < 0.001, uncorrected, k > 20. (C) Scatterplot depicting the relationship between the functional connectivity measure of the striatum–mPFC (positive > negative feedback) and age. (D) Scatterplot depicting the relationship between the functional connectivity measure of the striatum–mPFC (positive > negative feedback) and learning rate (α_neg).