Adolescent development of context-dependent stimulus-reward association memory and its neural correlates

Expression of learned stimulus-reward associations based on context is essential for regulation of behavior to meet situational demands. Contextual regulation improves during development, although the developmental progression of relevant neural and cognitive processes is not fully specified. We therefore measured neural correlates of flexible, contextual expression of stimulus-reward associations in pre/early-adolescent children (ages 9-13 years) and young adults (ages 19-22 years). After reinforcement learning using standard parameters, a contextual reversal manipulation was used whereby contextual cues indicated that stimulus-reward associations were the same as previously reinforced for some trials (consistent trials) or were reversed on other trials (inconsistent trials). Subjects were thus required to respond according to original stimulus-reward associations vs. reversed associations based on trial-specific contextual cues. Children and young adults did not differ in reinforcement learning or in relevant functional magnetic resonance imaging (fMRI) correlates. In contrast, adults outperformed children during contextual reversal, with better performance specifically for inconsistent trials. fMRI signals corresponding to this selective advantage included greater activity in lateral prefrontal cortex (LPFC), hippocampus, and dorsal striatum for young adults relative to children. Flexible expression of stimulus-reward associations based on context thus improves via adolescent development, as does recruitment of brain regions involved in reward learning and contextual expression of memory. HighlightsEarly-adolescent children and young adults were equivalent in reinforcement learning.Adults outperformed children in contextual expression of stimulus-reward associations.Adult advantages correlated with increased activity of relevant brain regions.Specific neurocognitive developmental changes support better contextual regulation.