The Neural Underpinnings of How Reward Associations Can Both Guide and Misguide Attention

Krebs, Ruth M.; Boehler, C. Nico; Egner, Tobias; Woldorff, Marty G. · 2011 · OpenAlex-citations

DOI: 10.1523/jneurosci.0732-11.2011

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Summary

This study investigates the neural mechanisms underlying how reward associations can both facilitate and disrupt attentional performance. While reward is typically viewed as a motivator that enhances behavior, prior research indicated that implicit reward associations in task-irrelevant dimensions can induce behavioral costs. The authors aimed to identify the specific brain regions responsible for these beneficial and detrimental effects using functional magnetic resonance imaging (fMRI) in humans. The researchers employed a reward-modulated Stroop task with 19 participants. Subjects were instructed to identify the ink color of presented words while ignoring their semantic meaning. Two ink colors were associated with monetary rewards (potential reward), while the other two were not. Crucially, the semantic meaning of incongruent words could implicitly refer to either the rewarded or non-rewarded ink colors, creating a task-irrelevant reward association. This design allowed the isolation of neural responses to relevant reward cues (ink color) and irrelevant reward cues (word meaning). Behavioral data were analyzed using repeated-measures ANOVAs, and fMRI data were processed using Statistical Parametric Mapping to identify voxel-wise differences in brain activity. Behavioral results confirmed that relevant reward associations facilitated performance, resulting in faster response times and fewer errors compared to non-rewarded trials. However, irrelevant reward associations induced significant behavioral detriments; responses were slower when incongruent words implicitly referred to rewarded colors compared to those referring to non-rewarded colors. Neurologically, relevant reward associations activated the nucleus accumbens (NAcc), a key region in the reward-anticipation circuit, with activity levels predicting behavioral facilitation. In contrast, irrelevant reward associations increased activity in the presupplementary motor area (pre-SMA). This pre-SMA activation was positively correlated with response slowing, suggesting it reflects the inhibition of automatic response tendencies triggered by salient but irrelevant reward-related words. Both conditions also engaged visual processing areas, specifically the fusiform gyrus, indicating that reward saliency transfers to irrelevant dimensions through shared visual coding mechanisms. The findings demonstrate that reward associations influence stimulus processing and response selection automatically, even when the reward cue is irrelevant to the task. The study identifies distinct neural pathways for the dual effects of reward: the NAcc mediates performance enhancement through reward anticipation, while the pre-SMA mediates performance disruption by managing conflict from irrelevant reward signals. These results highlight a "flipside" to reward-driven attention, where implicit associations can misguide attention and impair cognitive control, providing a neural explanation for how reward contexts can simultaneously aid and hinder behavioral performance.

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• attention selective divided