Common and distinct neural correlates of personal and vicarious reward: A quantitative meta-analysis

Abstract

Individuals experience reward not only when directly receiving positive outcomes (e.g., food or money), but also when observing others receive such outcomes. This latter phenomenon, known as vicarious reward, is a perennial topic of interest among psychologists and economists. More recently, neuroscientists have begun exploring the neuroanatomy underlying vicarious reward. Here we present a quantitative whole-brain meta-analysis of this emerging literature. We identified 25 functional neuroimaging studies that included contrasts between vicarious reward and a neutral control, and subjected these contrasts to an activation likelihood estimate (ALE) meta-analysis. This analysis revealed a consistent pattern of activation across studies, spanning structures typically associated with the computation of value (especially ventromedial prefrontal cortex) and mentalizing (including dorsomedial prefrontal cortex and superior temporal sulcus). We further quantitatively compared this activation pattern to activation foci from a previous meta-analysis of personal reward. Conjunction analyses yielded overlapping VMPFC activity in response to personal and vicarious reward. Contrast analyses identified preferential engagement of the nucleus accumbens in response to personal as compared to vicarious reward, and in mentalizing-related structures in response to vicarious as compared to personal reward. These data shed light on the common and unique components of the reward that individuals experience directly and through their social connections.

The dopaminergic reward system underpins gender differences in social preferences

“…Recent evidence suggests that dopaminergic activity is sensitive not only to rewards for oneself but to rewards for others as well 9 . The assumption that dopamine is sensitive to both self-and other-related outcomes is consistent with the finding that the striatum shows activation for both selfish and shared rewards [10][11][12][13][14][15] . The dopaminergic response may represent a net signal encoding the difference between the value of preferred and unpreferred rewards 8 .…”

Neurocomputational mechanisms of prosocial learning and links to empathy

“…Recent studies of sgACC function have found signals in this region relevant for social cognition and behavior including credit assignment (44), prosocial and moral behavior (6,16,45,46), the experience of positive affect (47), trust (48), social emotion (49), and vicarious reward (50,51). Moreover, there is evidence that the sgACC may signal PEs for self-reward but only when learning occurs at a specific level of abstraction beyond basic stimulus-response association (52).…”

“…For example, studies have suggested that other neurocognitive processes, in addition to simulation, may be important when processing vicarious information, particularly in the domain of positive affect (see ref. 51 for a metaanalysis and ref. 30 for review).…”

Prosocial deficits in behavioral variant frontotemporal dementia relate to reward network atrophy

“…Money, pleasant odors, attractive people, smiling faces, and appetitive cues all recruit the ventral striatum (Kuhn & Gallinat, 2012; Sescousse et al., 2013). During vicarious reward, despite the fact that observers do not directly receive rewards themselves, the ventral striatum is also active, which perhaps reflects its role in triggering the mutual positive feelings that arise from prosocial actions (Mobbs et al., 2009; Morelli et al., 2015). In bvFTD, atrophy in the right ventral striatum is common and has been associated with increased seeking of primary rewards (e.g., food and alcohol), suggesting that patients with bvFTD may be hyper‐reactive to certain types of nonsocial rewarding cues (Perry et al., 2014).…”

“…Shared positive feelings may foster prosocial behaviors by activating neural systems (i.e., ventral striatum, anterior cingulate cortex, medial orbitofrontal cortex, thalamus, amygdala, and anterior insula) that support reward processing (Berridge & Kringelbach, 2015; Haber & Knutson, 2010). Prosocial behaviors including altruistic giving (e.g., spending money on others and giving to charities), empathic validation, emotional support, and cooperation activate reward network hubs such as the ventral striatum, among others (Declerck, Boone, & Emonds, 2013; Dunn, Aknin, & Norton, 2008; Harbaugh, Mayr, & Burghart, 2007; Inagaki & Eisenberger, 2012; Izuma, Saito, & Sadato, 2010; Morelli, Torre, & Eisenberger, 2014), that support reward processing as well as emotion and empathy more broadly (Cloutier, Heatherton, Whalen, & Kelley, 2008; Decety & Jackson, 2004; Mobbs et al., 2009; Morelli, Sacchet, & Zaki, 2015; Sescousse, Caldu, Segura, & Dreher, 2013). …”