Relief as a reward: hedonic and neural responses to safety from pain

Abstract

Relief fits the definition of a reward. Unlike other reward types the pleasantness of relief depends on the violation of a negative expectation, yet this has not been investigated using neuroimaging approaches. We hypothesized that the degree of negative expectation depends on state (dread) and trait (pessimism) sensitivity. Of the brain regions that are involved in mediating pleasure, the nucleus accumbens also signals unexpected reward and positive prediction error. We hypothesized that accumbens activity reflects the level of negative expectation and subsequent pleasant relief. Using fMRI and two purpose-made tasks, we compared hedonic and BOLD responses to relief with responses during an appetitive reward task in 18 healthy volunteers. We expected some similarities in task responses, reflecting common neural substrates implicated across reward types. However, we also hypothesized that relief responses would differ from appetitive rewards in the nucleus accumbens, since only relief pleasantness depends on negative expectations. The results confirmed these hypotheses. Relief and appetitive reward task activity converged in the ventromedial prefrontal cortex, which also correlated with appetitive reward pleasantness ratings. In contrast, dread and pessimism scores correlated with relief but not with appetitive reward hedonics. Moreover, only relief pleasantness covaried with accumbens activation. Importantly, the accumbens signal appeared to specifically reflect individual differences in anticipation of the adverse event (dread, pessimism) but was uncorrelated to appetitive reward hedonics. In conclusion, relief differs from appetitive rewards due to its reliance on negative expectations, the violation of which is reflected in relief-related accumbens activation.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1. Experimental design and behavioural ratings.

A: Overview of relief and appetitive reward task design and timing of events. Each relief task trial began with a 6-second anticipatory period, in which participants expected intense pain. 50% of anticipation periods were followed by intense pain for 5 seconds; in the remaining events a safety cue was presented on the screen for 5 seconds. In the appetitive reward task, participants imagined pleasant scenarios (activities involving appetitive rewards) or neutral scenarios according to the text on the screen. The graphs in panel B depict behavioural ratings from the relief and the appetitive reward tasks. ** denotes p

Figure 2. Task-induced brain activation patterns.

A: Main effect of relief task (red) and appetitive reward task (yellow). B: The overlap between the two tasks (green) and between-tasks contrasts (light and dark blue). MRI images are overlaid on the normalised average of the whole group's structural scans, and thresholded using a cluster-based approach with Z>2.3, p

Figure 3. Correlation and regression analyses.

Hedonic ratings of relief were significantly positively correlated with ratings of anticipatory dread in the relief task (A) as well as with hedonic ratings from the appetitive reward task (B). As hypothesised, relief hedonics also significantly covaried with optimism scores, such that more pessimistic participants reported higher relief pleasantness (C). Panel D shows a significant association between relief hedonics and accumbens (NAc) activation in the relief task. In contrast, hedonic ratings in the reward task did not covary with NAc activity; these ratings correlated with voxels in the rACC/mPFC region (E).

Figure 4. Pessimism and BOLD response to safety.

A: Consistent with the observed effect of pessimism on relief hedonics, pessimism scores also correlated with voxels in the left and right NAc in the relief task. To illustrate this relationship, we split participants into more pessimistic and more optimistic groups using the median score on the LOT-R. The more pessimistic group (n = 7) showed higher relief pleasantness (p = 0.035, one-tailed), and the two groups showed opposite BOLD responses in the left and right nucleus accumbens (NAc) during unexpected safety (B). In contrast, both groups showed positive NAc responses during the pleasant scenarios in the appetitive reward task (C). Duration of stimuli are indicated by the white horizontal bars. Error bars indicate SEM. The MRI image shows the standard MNI brain.