The Influence of Vicarious Fear-Learning in "Infecting" Reactive Action Inhibition

Abstract

Since the dawn of cognitive neuroscience, emotions have been recognized to impact on several executive processes, such as action inhibition. However, the complex interplay between emotional stimuli and action control is not yet fully understood. One way to measure inhibitory control is the stop-signal task (SST), which estimates the ability to cancel outright an action to the presentation of a stop signal by means of the stop-signal reaction times (SSRTs). Impaired as well as facilitated action control has been found when faced with intrinsic emotional stimuli as stop signals in SSTs. Here, we aimed at investigating more deeply the power of negative stimuli to influence our action control, testing the hypothesis that a previously neutral stimulus [i.e., the image of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2)], which has been conditioned through vicarious fear learning, has the same impact on reactive action inhibition performance as an intrinsically negative stimulus (i.e., a fearful face or body). Action control capabilities were tested in 90 participants by means of a SST, in which the stop signals were represented by different negative stimuli. Results showed that the SARS-CoV-2 image enhanced the ability to suppress an ongoing action similarly to observing fearful facial expressions or fearful body postures. Interestingly, we found that this effect was predicted by impulsivity traits: for example, the less self-control the participants had, the less they showed emotional facilitation for inhibitory performance. These results demonstrated that vicarious fear learning has a critical impact on cognitive abilities, making a neutral image as threatening as phylogenetically innate negative stimuli and able to impact on our behavioral control.

Keywords: SARS-CoV-2; action inhibition; negative emotion; stop-signal task (SST); vicarious fear-learning.

FIGURE 1

Stimuli used as stop-signal stimuli. In the SARS-CoV-2 group stimuli consisted of a stylized black and white image of the virus COVID-19 and an image of a black and white fractal with irregular outlines, acting as control neutral stimulus. In the Fear-Face group stimuli consisted of two different face pictures, showing a fear and neutral expression, which were selected from the Ekman set (Ekman and Friesen, 1976). In the Fear-Body group, stimuli consisted of two different body pictures with fearful and neutral expression, previously used in Borgomaneri et al. (2015a,,, .

FIGURE 2

Sequence of trials in the stop-signal task (SST). The experimental task includes both Go- and Stop-trials (Lappin and Eriksen, 1966; Logan and Cowan, 1984; Logan et al., 2014; Verbruggen et al., 2019). Participants perform a short practice block and, immediately afterward, four experimental blocks. Each block includes a total of 128 trials, of which 96 are Go-trials (75%) and 32 are Stop-trials (25%). In Go-trials, participants respond to the Go-task (i.e., the direction of the arrow that appears on the screen) by pressing the corresponding arrow key on the keyboard. In Stop-trials, the arrow is followed by a “Stop” signal after a variable stop-signal delay (FIX, fixation duration; SSD, stop-signal delay; ITI, intertrial interval), instructing participants to suppress the imminent Go response. The initial value of the SSD was set to 150 ms and adjusted individually and dynamically throughout the experiment (i.e., staircase procedure), so that, if participants successfully inhibited their response on a Stop-trial, the SSD was increased by 50 ms in a subsequent Stop-trial, while if they failed to withhold their motor response, the SSD was reduced by 50 ms in a subsequent Stop-trial.

FIGURE 3

Bar graph of the experimental results. In (A) the graph shows the mean stop-signal delay (SSD), demonstrating that negative emotional content of stimuli influenced the participant’s action execution leading to a specific differentiation of SSD, given the successful staircase procedure. In (B) the graph shows the mean stop-signal reaction time (SSRT), demonstrating that participants showed a better inhibitory process when facing negative Stop-signals as compared to neutral ones, regardless of the group. Asterisks indicate significant comparisons (p < 0.05), and error bars represent SEM. Asterisks indicate significant comparisons.

FIGURE 4

Significant correlation between non-planning impulsivity score (a subscale of the BIS-11 questionnaire) and SSRT index (calculated as Negative minus Neutral SSRT) in the three groups. Across participants, a significant linear relationship was observed, indicating that participants with higher levels of non-planned impulsivity showed a lower inhibitory performance improvement during the negative emotional stop conditions, with respect to their neutral counterparts.