Arousal-Biased Competition Explains Reduced Distraction by Reward Cues Under Threat

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Anxiety is an adaptive neural state that promotes rapid responses under heightened vigilance when survival is threatened. Anxiety has consistently been found to potentiate the attentional processing of physically salient stimuli. However, a recent study demonstrated that a threat manipulation reduces attentional capture by reward-associated stimuli, suggesting a more complex relationship between anxiety and the control of attention. The mechanisms by which threat can reduce the distracting quality of stimuli are unknown. In this study, using functional magnetic resonance imaging on human subjects, we examined the neural correlates of attention to previously reward-associated stimuli with and without the threat of unpredictable electric shock. We replicate enhanced distractor-evoked activity throughout the value-driven attention network in addition to enhanced stimulus-evoked activity generally under threat. Importantly, these two factors interacted such that the representation of previously reward-associated distractors was particularly pronounced under threat. Our results from neuroimaging fit well with the principle of arousal-biased competition, although such effects are typically associated with behavioral measures of increased attention to stimuli that already possess elevated attentional priority. The findings of our study suggest that arousal-biased competition can be leveraged to support more efficient ignoring of reward cues, revealing new insights into the functional significance of arousal-biased competition as a mechanism of attentional control, and provide a mechanistic explanation of how threat reduces attention to irrelevant reward information.

Significance Statement Anxiety disorders are the most common mental illnesses in the United States. Anxiety affects how we direct our attention, which plays an important role in both adaptive and maladaptive responses to threat, but our understanding of the mechanisms underlying this relationship is limited. Here, we used neuroimaging to explore the mechanisms by which threat modulates attention to reward-related stimuli. We find that experimentally-induced anxiety interacts with the neural network associated with attentional processing of valuable stimuli, enhancing the strength with which such stimuli are represented, but behaviorally results in a reduced tendency to look at these stimuli. Our findings reveal a novel relationship between threat and attention in which enhanced stimulus-evoked activity under threat can be leveraged to facilitate ignoring.

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