The Protective Effects of Perceived Control During Repeated Exposure to Aversive Stimuli

Abstract

The ability to perceive and exercise control is a major contributor to our mental and physical wellbeing. When faced with uncontrollable aversive stimuli, organisms develop heightened anxiety and become unwilling to exert effort to avoid the stimuli. In contrast, when faced with controllable aversive stimuli, organisms demonstrate behavioral vigor via avoidance attempts toward trying to seek and exercise control over the environment. As such, controllability confers protective effects against reduced avoidance motivation trigged by aversive environments. These observations beg the question of whether controllability can be potent enough to reverse passivity following repeated exposure to uncontrollable aversive stimuli and how this protective effect is encoded neurally. Human participants performed a Control in Aversive Domain (CAD) task where they were first subjected to a series of repeated uncontrollable aversive stimuli (i.e., aversive tones) across several contexts that were followed by a series of controllable aversive stimuli in a novel context. Faced with persistent uncontrollability, participants significantly reduced their avoidance attempts over time and biased toward giving up. However, the subsequent presence of controllability rescued participants' avoidance behavior. Strikingly, participants who responded more strongly to the protective effects of control also had greater ventromedial prefrontal cortical (vmPFC) activation-a region previously observed to be associated with encoding the subjective value of control. Taken together, these findings highlighted the protective effect conferred by perceived control against passivity and offered insights into the potential role of the vmPFC in controllable environments, with implications for understanding the beneficial influence of perceived control on adaptive behavior.

Keywords: avoidance behavior; learned helplessness; passivity; perceived control; ventromedial prefrontal cortex.

FIGURE 1

Experimental timeline of Control in Aversive Domain (CAD) task. (A) The CAD task consisted of three phases. The first phase comprised the exposure trials where participants responded to uncontrollable cues paired with either an aversive (4,000 Hz) or neutral (500 Hz) tone. The second phase comprised the uncontrollable trials where participants experienced a series of uncontrollable aversive tones (4,000 Hz) represented by a different cue compared to the exposure trials. The last phase comprised the controllable trials where participants were given a series of controllable aversive tones (4,000 Hz) paired with yet another novel cue. (B) Example trial. In each trial, regardless of the experimental phase, participants were presented a cue (all experimental cues shown for completeness) displayed for 4 s. During the cue presentation for each trial, participants had the option to either press the AVOID or GIVE-UP button. By choosing to press the AVOID button, participants could try to control and avoid the associated tone. A successful AVOID button press yielded no tone presentation whereas a failed AVOID button press yielded 4 s of tone. By choosing the GIVE-UP button, participants would receive a guaranteed 2 s of the associated tone. The cue and tone periods respectively ended with a jittered interstimulus and intertrial interval signaled by a crosshair.

FIGURE 2

Behavioral findings. (A) Exposure phase. Participants’ avoidance behavior revealed a significant main effect of time. Pairwise comparisons showed that this significant effect was driven by the marked decrease in AVOID button presses unilaterally present in the aversive but not neutral trials. (B) Uncontrollable and controllable phases. Participants significantly increased their avoidance behavior in the controllable phase when compared to the uncontrollable phase. (C) We examined participants’ changes in avoidance behavior between the early and late aversive exposure trials compared to the same changes in behavior across exposure (combined trials) and uncontrollable trials. We found that participants who showed greater decrease in their avoidance behavior from the early to late aversive exposure trials (i.e., larger x-axis) also showed greater decrease in their avoidance behavior from the aversive exposure to uncontrollable trials (i.e., larger y-axis). (D) We investigated the relationship between the proportion of avoidance behavior in the exposure and controllable phases and found that participants who made more avoidance presses in the exposure phase also subsequently made more avoidance presses in the controllable phase. Result remained significant even after removing outllier. *p < 0.05.

FIGURE 3

Neural correlates for uncontrollable cues. To examine differences in neural activation between the uncontrollable and controllable phases, we conducted a GLM contrasting the uncontrollable—controllable trials. We observed activity in the amygdala, insula, cingulate cortex and caudate after correcting for multiple comparisons.

FIGURE 4

Correlation of avoidance behavior and neural activity. We examined the relationship between vmPFC activity in the controllable—uncontrollable cue contrast and participants’ changes in avoidance behavior between the two phases. Using a functional mask (shown in the right insert) created from the peak coordinate (peak MNI_{x, y, z} = −6, 32, −14) reported in Wang and Delgado (2019), we extracted the peak activation and correlated them with participants’ change in avoidance attempts from the controllable to uncontrollable phase. We found that participants with a larger vmPFC peak activation also had a bigger increase in avoidance behavior in the controllable trials.