Differential effects of acute stress on anticipatory and consummatory phases of reward processing

Abstract

Anhedonia is one of the core symptoms of depression and has been linked to blunted responses to rewarding stimuli in striatal regions. Stress, a key vulnerability factor for depression, has been shown to induce anhedonic behavior, including reduced reward responsiveness in both animals and humans, but the brain processes associated with these effects remain largely unknown in humans. Emerging evidence suggests that stress has dissociable effects on distinct components of reward processing, as it has been found to potentiate motivation/'wanting' during the anticipatory phase but reduce reward responsiveness/'liking' during the consummatory phase. To examine the impact of stress on reward processing, we used a monetary incentive delay (MID) task and an acute stress manipulation (negative performance feedback) in conjunction with functional magnetic resonance imaging (fMRI). Fifteen healthy participants performed the MID task under no-stress and stress conditions. We hypothesized that stress would have dissociable effects on the anticipatory and consummatory phases in reward-related brain regions. Specifically, we expected reduced striatal responsiveness during reward consumption (mirroring patterns previously observed in clinical depression) and increased striatal activation during reward anticipation consistent with non-human findings. Supporting our hypotheses, significant Phase (Anticipation/Consumption)×Stress (Stress/No-stress) interactions emerged in the putamen, nucleus accumbens, caudate and amygdala. Post hoc tests revealed that stress increased striatal and amygdalar activation during anticipation but decreased striatal activation during consumption. Importantly, stress-induced striatal blunting was similar to the profile observed in clinical depression under baseline (no-stress) conditions in prior studies. Given that stress is a pivotal vulnerability factor for depression, these results offer insight to better understand the etiology of this prevalent disorder.

Keywords: anticipation; basal ganglia; consumption; monetary incentive delay; reward; stress.

Fig. 1

Study procedure (A) and Monetary Incentive Delay task design (B)

Fig. 2

Skin conductance levels (A), Affective ratings (B) and reaction times (C) across stress (averaged runs 2 & 3) and no-stress (averaged runs 1 & 4) runs. Means and SE are shown.

Fig. 3

Skin Conductance Levels across all four runs. Means and SE are shown.

Fig. 4

Subscale ratings across all four runs. Mean ratings for Stressed (A), Anxious (B) Happy (C), and In Control (D) are shown. Mean and SE are shown.

Fig. 5

Main effect of task during anticipation (A) and consumption (B). Fig. 5A shows regions with significant results for the reward vs. no-incentive cue contrast (p < 0.05 FWE cluster-corrected) in red overlaid onto the 2 mm MNI standard brain. Fig. 5B shows regions with significant results for the gain vs. no-change feedback contrast (p < 0.05 FWE cluster-corrected) in yellow overlaid onto the 2 mm MNI standard brain.

Fig. 6

Parameter estimates extracted from functional ROIs during anticipation and consumption in the putamen (A), nucleus accumbens (B), right caudate (C), left caudate (D) and amygdala (E) during stress (Run 1) and no-stress (Run 2) conditions. Means and SE are shown.