Primary and Secondary Rewards Differentially Modulate Neural Activity Dynamics during Working Memory

Beck, Stefanie; Locke, Hannah; Savine, Adam C.; Jimura, Koji; Braver, Todd S. · 2010 · OpenAlex-citations

DOI: 10.1371/journal.pone.0009251

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Summary

This study investigates how different types of motivational incentives—primary (liquid) versus secondary (monetary) rewards—modulate neural activity dynamics during working memory tasks. While previous research established that rewards enhance cognitive control, it remained unclear whether the neural mechanisms underlying these effects depend on the category of reward or if they operate through uniform pathways. The authors aimed to dissociate sustained (tonic) from transient (phasic) neural responses to determine if primary and secondary rewards engage distinct neural circuits despite producing similar behavioral improvements. The researchers employed a within-subjects functional MRI design with 31 participants performing a delayed item recognition working memory task. Incentives were manipulated across blocks: monetary bonuses were awarded post-session (secondary reward), while drops of apple juice were delivered directly into the mouth during trials (primary reward). To isolate temporal dynamics, the design combined block-level incentive conditions with trial-by-trial variations in reward magnitude (no, low, or high). This mixed blocked/event-related design allowed the decomposition of brain activation into sustained state effects and transient event-related responses. Data analysis utilized region-of-interest (ROI) approaches focusing on canonical cognitive control networks (prefrontal and parietal cortices) and reward processing networks (subcortical structures like the striatum and amygdala). Behaviorally, both monetary and liquid incentives significantly improved reaction times compared to baseline, with no significant difference in performance enhancement between the two reward types. However, neural activity patterns differed markedly. Monetary rewards elicited sustained activation increases primarily in right-lateralized cognitive control regions, including the anterior prefrontal cortex, dorsolateral prefrontal cortex, and parietal cortex. In contrast, liquid rewards did not produce sustained activation in these cognitive control areas. Instead, liquid incentives shifted transient activation from a reactive pattern (probe-based) to a proactive pattern (cue-based) in the same regions. Furthermore, liquid rewards uniquely induced sustained activation in subcortical reward regions, including the amygdala, dorsal striatum, and nucleus accumbens, whereas monetary rewards showed sustained activity in the caudate but not these specific subcortical areas. These findings demonstrate an anatomical double dissociation in the locus of sustained activation, suggesting that primary and secondary rewards produce equivalent behavioral enhancements through distinct neural mechanisms. Monetary rewards appear to engage a tonic, sustained mode of cognitive control, while liquid rewards promote a more flexible, transient proactive control strategy alongside heightened subcortical engagement. This highlights the flexibility of cognitive control systems and indicates that the neural implementation of motivation is category-specific, challenging assumptions that motivational incentives exert domain-general effects regardless of reward type.

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• executive function