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

Abstract

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 (fMRI) 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 (VDAN) 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 (ABC), 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 ABC can be leveraged to support more efficient ignoring of reward cues, revealing new insights into the functional significance of ABC as a mechanism of attentional control, and provide a mechanistic explanation of how threat reduces attention to irrelevant reward information.

How Does Threat Modulate the Motivational Effects of Reward on Attention?

“…The extent to which threat modulates attentional processes in the auditory system remains underexplored. Our threat manipulation exactly mirrored that which has consistently both impaired and facilitated the control of attention in the visual domain (Kim & Anderson, 2020a, 2020cKim et al, 2021a), and so it is unlikely that the lack of evidence for an interaction with threat in the present study was the result of an ineffective manipulation of threat. The effect of reward on attention in the present study was highly robust, and so there was also ample space for threat to modulate such reward-related priority.…”

“…We a priori chose to complete a betweensubjects design due to the relatively stronger behavioral differences reported compared to a within-subjects design (Kim & Anderson, 2020c). Furthermore, although we have verified that our threat of shock protocol induces a negative arousal effect using pupil size analyses (Kim & Anderson, 2020a) and self-report questionnaires (e.g., Kim & Anderson, 2020a, 2021c, this current dataset lacks a manipulation check that confirms a significant change in arousal within the threat group.…”

“…In the no-threat group, we again identified a significant difference between the high and no reward conditions, t(23) = 5.10, p < .001, d = 0.794, and the high and low conditions, t(23) = 3.18, p = .004, d = 0.517, but no significant differences between the low and no reward conditions, t(23) = 1.75, p = .093. Given that we did not find evidence to reject the null hypothesis concerning the modulatory influence of threat (H 0 : threat does not interact with reward) as previously seen in studies measuring involuntary attentional capture (Kim & Anderson, 2020a, 2020c, we evaluated the evidence for the alternative hypothesis (H A : threat interacts with reward) using a Bayesian ANOVA in JASP over RT. We found the preferred model to include just the effect of reward, BF M = 7.941, corroborating our prior findings from the main effect of value from the repeated-measures ANOVA.…”

“…Furthermore, a state of heightened vigilance has been shown to reduce task-related errors in a Go/No-Go task, again demonstrating that threat facilitates improvements in information processing and benefits task performance (Grillon et al, 2017). In contrast, in the context of the influence of reward on attention, threat has been shown to suppress value-driven attentional biases and reduce attentional capture by previously reward-associated stimuli (Kim & Anderson, 2020a, 2020c. Thus, it is plausible that the null results in the present study are a result of two offsetting attentional control mechanisms in which threat facilitates motivated attention more broadly while suppressing the more automatic influence of learned value on information processing.…”

Bicyclist-evoked arousal and greater attention to bicyclists independently promote safer driving

“…Using self-report measures of state anxiety, highly anxious participants have shown increased attentional biases toward physically salient stimuli (e.g., Esterman et al, 2013 ; Moser et al, 2012 ). Furthermore, the threat of unpredictable electric shock has been shown to induce negative arousal, which elevates the attentional priority afforded to physically salient stimuli and reduces the attentional priority afforded to previously reward-associated stimuli (Kim & Anderson, 2020a , b ; see also Mather & Sutherland, 2011 ; Sutherland & Mather, 2012 , 2015 ). Furthermore, a state of negative arousal induced by a threat-of-shock manipulation has been shown to facilitate goal-directed attentional control and improve task performance (Kim et al, 2021 ).…”