Development of corticostriatal connectivity constrains goal-directed behavior during adolescence

Insel, Catherine; Kastman, Erik K.; Glenn, Catherine R.; Somerville, Leah H. · 2017 · Crossref

DOI: 10.1038/s41467-017-01369-8

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Summary

This study investigates the developmental trajectory of goal-directed behavior, specifically examining how individuals integrate value-based goals to modulate cognitive performance. While adults typically enhance cognitive control in high-stakes situations, it remains unclear whether adolescents possess this capacity or if their performance is constrained by ongoing neurodevelopment. The authors hypothesized that the late maturation of corticostriatal connectivity limits adolescents' ability to selectively titrate cognitive resources according to environmental demands. To test this, researchers conducted a functional magnetic resonance imaging (fMRI) study with participants aged 13 to 20. Participants performed a value-contingent go/no-go task ("Planets task") requiring flexible action selection under varying financial stakes. High stakes involved higher rewards for correct responses and larger penalties for errors compared to low stakes. Behavioral performance was measured using d-prime (d′), and neural mechanisms were assessed using psychophysiological interaction (PPI) analyses to evaluate functional connectivity between the ventral striatum (VS) and prefrontal cortex. Behavioral results revealed a significant interaction between age and stakes. Adults (ages 19–20) significantly improved performance during high-stakes conditions, whereas younger adolescents showed no such improvement. Neuroimaging data indicated that high stakes elicited enhanced recruitment of corticostriatal regions, including the VS, dorsal striatum, and ventrolateral prefrontal cortex (vlPFC). Crucially, PPI analyses demonstrated that connectivity between the VS and vlPFC increased with age during high-stakes trials. In contrast, within-striatum connectivity decreased with age. Mediation analysis confirmed that the age-related increase in VS–vlPFC connectivity accounted for the emergence of stakes-based performance improvements. This mediation held even after controlling for demographic factors, reaction times, and structural brain differences. Additionally, subjective valuation of stakes was consistent across all age groups, ruling out differential motivation as a cause for behavioral differences. The findings demonstrate that the capacity to selectively enhance cognitive control in high-stakes contexts emerges late in adolescence, mediated by the maturation of long-range corticostriatal connectivity. This suggests that adolescents may not benefit from high-stakes incentives to the same degree as adults due to incomplete neural circuit development. These results clarify inconsistent prior literature on adolescent incentive processing and highlight the specific neural mechanisms underlying the development of optimal, value-guided goal-directed behavior.

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• executive function