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

It is commonly accepted that reward is an effective motivator of behavior, but little is known about potential costs resulting from reward associations. Here, we used functional magnetic resonance imaging (fMRI) to investigate the neural underpinnings of such reward-related performance-disrupting effects in a reward-modulated Stroop task in humans. While reward associations in the task-relevant dimension (i.e., ink color) facilitated performance, behavioral detriments were found when the task-irrelevant dimension (i.e., word meaning) implicitly referred to reward-predictive ink colors. Neurally, only relevant reward associations invoked a typical reward-anticipation response in the nucleus accumbens (NAcc), which was in turn predictive of behavioral facilitation. In contrast, irrelevant reward associations increased activity in a medial prefrontal motor-control-related region, namely the presupplementary motor area (pre-SMA), which likely reflects the preemption and inhibition of automatic response tendencies that are amplified by irrelevant reward-related words. This view was further supported by a positive relationship between pre-SMA activity and pronounced response slowing in trials containing reward-related as compared with reward-unrelated incongruent words. Importantly, the distinct neural processes related to the beneficial and detrimental behavioral effects of reward associations appeared to arise from preferential-coding mechanisms in visual-processing areas that were shared by the two stimulus dimensions, suggesting a transfer of reward-related saliency to the irrelevant dimension, but with highly differential behavioral and neural ramifications. More generally, the data demonstrate that even entirely irrelevant reward associations can influence stimulus-processing and response-selection pathways relatively automatically, thereby representing an important flipside of reward-driven performance enhancements.