Threat expectation does not improve perceptual discrimination despite causing heightened priority processing in the frontoparietal network

Abstract

Threat cues have been widely shown to elicit increased sensory and attentional neural processing. However, whether this enhanced recruitment leads to measurable behavioral improvements in perception is still in question. Here we adjudicate between two opposing theories: that threat cues do or do not enhance perceptual sensitivity. We created threat stimuli by pairing one direction of motion in a random dot kinematogram with an aversive sound. While in the MRI scanner, 46 subjects (both men and women) completed a cued (threat/safe/neutral) perceptual decision-making task where they indicated the perceived motion direction of each moving dots stimulus. We found strong evidence that threat cues did not increase perceptual sensitivity compared to safe and neutral cues. This lack of improvement in perceptual decision-making ability occurred despite the threat cue resulting in widespread increases in frontoparietal BOLD activity, as well as increased connectivity between the right insula and the frontoparietal network. These results call into question the intuitive claim that expectation automatically enhances our perception of threat, and highlight the role of the frontoparietal network in prioritizing the processing of threat-related environmental cues. Significance StatementThreatening information receives enhanced priority processing in the brain. Evidence of increased neural activity to threat has fostered the current view that such selective processing leads to a boost in perception, suggesting that motivationally relevant top-down effects can directly change what we see. In the real world, danger is often preceded by an environmental cue that predicts its imminent approach. Here we used an aversive conditioning paradigm to test whether threat cues can change subjects ability to visually distinguish between threat and safe stimuli. Our results provide strong evidence for the lack of an effect of threat expectation on perceptual sensitivity, supporting the theory that perception is impenetrable by top-down cognitive influences despite robust neural attentional priority.