One fundamental question concerning brain reward mechanisms is to determine how reward-related activity is influenced by the nature of rewards. Here, we review the neuroimaging literature and explicitly assess to what extent the representations of primary and secondary rewards overlap in the human brain. To achieve this goal, we performed an activation likelihood estimation (ALE) meta-analysis of 87 studies (1452 subjects) comparing the brain responses to monetary, erotic and food reward outcomes. Those three rewards robustly engaged a common brain network including the ventromedial prefrontal cortex, ventral striatum, amygdala, anterior insula and mediodorsal thalamus, although with some variations in the intensity and location of peak activity. Money-specific responses were further observed in the most anterior portion of the orbitofrontal cortex, supporting the idea that abstract secondary rewards are represented in evolutionary more recent brain regions. In contrast, food and erotic (i.e. primary) rewards were more strongly represented in the anterior insula, while erotic stimuli elicited particularly robust responses in the amygdala. Together, these results indicate that the computation of experienced reward value does not only recruit a core "reward system" but also reward type-dependent brain structures.
To ensure their survival, animals exhibit a number of reward-directed behaviors, such as foraging for food or searching for mates. This suggests that a core set of brain regions may be shared by many species to process different types of rewards. Conversely, many new brain areas have emerged over the course of evolution, suggesting potential specialization of specific brain regions in the processing of more recent rewards such as money. Here, using functional magnetic resonance imaging in humans, we identified the common and distinct brain systems processing the value of erotic stimuli and monetary gains. First, we provide evidence that a set of neural structures, including the ventral striatum, anterior insula, anterior cingulate cortex, and midbrain, encodes the subjective value of rewards regardless of their type, consistent with a general hedonic representation. More importantly, our results reveal reward-specific representations in the orbitofrontal cortex (OFC): whereas the anterior lateral OFC, a phylogenetically recent structure, processes monetary gains, the posterior lateral OFC, phylogenetically and ontogenetically older, processes more basic erotic stimuli. This dissociation between OFC representations of primary and secondary rewards parallels current views on lateral prefrontal cortex organization in cognitive control, suggesting an increasing trend in complexity along a postero-anterior axis according to more abstract representations. Together, our results support a modular view of reward value coding in the brain and propose that a unifying principle of postero-anterior organization can be applied to the OFC.
Pathological gambling is an addictive disorder characterized by a persistent and compulsive desire to engage in gambling activities. This maladaptive behaviour has been suggested to result from a decreased sensitivity to experienced rewards, regardless of reward type. Alternatively, pathological gambling might reflect an imbalance in the sensitivity to monetary versus non-monetary incentives. To directly test these two hypotheses, we examined how the brain reward circuit of pathological gamblers responds to different types of rewards. Using functional magnetic resonance imaging, we compared the brain responses of 18 pathological gamblers and 20 healthy control subjects while they engaged in a simple incentive task manipulating both monetary and visual erotic rewards. During reward anticipation, the ventral striatum of pathological gamblers showed a differential response to monetary versus erotic cues, essentially driven by a blunted reactivity to cues predicting erotic stimuli. This differential response correlated with the severity of gambling symptoms and was paralleled by a reduced behavioural motivation for erotic rewards. During reward outcome, a posterior orbitofrontal cortex region, responding to erotic rewards in both groups, was further recruited by monetary gains in pathological gamblers but not in control subjects. Moreover, while ventral striatal activity correlated with subjective ratings assigned to monetary and erotic rewards in control subjects, it only correlated with erotic ratings in gamblers. Our results point to a differential sensitivity to monetary versus non-monetary rewards in pathological gambling, both at the motivational and hedonic levels. Such an imbalance might create a bias towards monetary rewards, potentially promoting addictive gambling behaviour.
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