Distracted by danger: Temporal and spatial dynamics of visual selection in the presence of threat

Abstract

Threatening stimuli are known to influence attentional and visual processes in order to prioritize selection. For example, previous research showed faster detection of threatening relative to nonthreatening stimuli. This has led to the proposal that threatening stimuli are prioritized automatically via a rapid subcortical route. However, in most studies, the threatening stimulus is always to some extent task relevant. Therefore, it is still unclear if threatening stimuli are automatically prioritized by the visual system. We used the additional singleton paradigm with task-irrelevant fear-conditioned distractors (CS+ and CS-) and indexed the time course of eye movement behavior. The results demonstrate automatic prioritization of threat. First, mean latency of saccades directed to the neutral target was increased in the presence of a threatening (CS+) relative to a nonthreatening distractor (CS-), indicating exogenous attentional capture and delayed disengagement of covert attention. Second, more error saccades were directed to the threatening than to the nonthreatening distractor, indicating a modulation of automatically driven saccades. Nevertheless, cumulative distributions of the saccade latencies showed no modulation of threat for the fastest goal-driven saccades, and threat did not affect the latency of the error saccades to the distractors. Together these results suggest that threatening stimuli are automatically prioritized in attentional and visual selection but not via faster processing. Rather, we suggest that prioritization results from an enhanced representation of the threatening stimulus in the oculomotor system, which drives attentional and visual selection. The current findings are interpreted in terms of a neurobiological model of saccade programming.

The influence of emotional stimuli on the oculomotor system: A review of the literature

“…1b). With this paradigm, it was found that endogenously driven saccades to the target are slowed more by a threatening distractor than by a nonthreatening distractor (Hopkins, Helmstetter, & Hannula, 2016;Mulckhuyse & Dalmaijer, 2016). These results indicate that the threatening distractor captured covert attention automatically and thereby delayed the programming of a saccade to a different location.…”

“…Most studies that investigated the effect of attentional capture by an emotional stimulus on oculomotor behavior found faster saccades to the emotional stimulus, reflecting enhanced attentional capture (Bannerman, Milders, de Gelder, et al, 2009;, 2010a, 2010bNummenmaa et al, 2009;Schmidt et al 2015Schmidt et al , 2017, slower saccades away from an emotional stimulus, reflecting delayed attentional disengagement (Bannerman et al, 2010a(Bannerman et al, , 2010bBelopolsky et al, 2011;Hopkins et al, 2016;Mulckhuyse & Dalmaijer, 2016;Schmidt et al, 2015Schmidt et al, , 2017, stronger deviations toward an emotional distractor (McSorley & van Reekum, 2013;Mulckhuyse et al, 2013), or away from an emotional distractor (Mulckhuyse et al, 2013;Nummenmaa et al, 2009;Schmidt et al, 2012). However, because of the set-up of most studies, emotional attention is never isolated from endogenous and exogenous attention, but rather most studies show an integration of emotion with endogenous or exogenous attentional processes (see also Brosch, Pourtois, Sander, & Vuilleumier, 2011).…”

“…Exogenous attentional capture, most especially, seems to be enhanced by emotion (Carretié, 2014). For instance, studies that did find an effect of emotion often presented the emotional stimulus as a sudden onset (Bannerman, Milders, de Gelder, et al, 2009;, 2010a, 2010bHopkins et al, 2016;Mulckhuyse & Dalmaijer, 2016;Schmidt et al, 2015Schmidt et al, , 2017, whereas in visual search studies that did not find an effect of emotion, the stimulus display including the target and distractor were presented together and for relatively long durations (DeVue & Grimshaw, 2017;Hunt et al, 2007a). In other words, there was no additional luminance transient present together with the emotional signal.…”

“…Besides the specific role of the amygdala in processing emotional pictures, the amygdala is also known to be essential in processing fear-conditioned stimuli (Davis & Whalen, 2001;LeDoux, 2000;Sehlmeyer et al, 2009). In fear conditioning, a stimulus, either a biologically relevant stimulus, such as a face (e.g., Armony & Dolan, 2002), or a biologically neutral stimulus, such as a specific color (e.g., Mulckhuyse & Dalmaijer, 2016), is associated with an aversive event, such as a loud noise or an electric shock to the finger (see Fig. 1a).…”

The time course of attentional bias to cues of threat and safety

“…Since saccade trajectories have been shown to indicate the amount of spatial attention that is allocated to a certain location (Van der Stigchel, Meeter, & Theeuwes, 2006), the results suggest a stronger attentional capture by fear-conditioned stimuli as compared to neutral ones. In a recent study, Mulckhuyse and Dalmaijer (2015) also demonstrated oculomotor capture by distractors that were previously associated with threat. Moreover, the presence of such distractors increased the latency of saccades to the target, suggesting that these distractors captured covert attention.…”