Review articleNeural signatures of prosocial behaviors
Introduction
Prosociality refers to behaviors that are intended to benefit others at a cost to the self (de Waal, 2008d; Jensen, 2016). Prosocial behaviors comprise a broad range of acts, which include caring, sharing, donating, helping, and volunteering (Dovidio, 2001; Padilla-Walker and Carlo, 2014; Penner et al., 2005). Three aspects are central to prosocial behaviors: (i) an agent intentionally carries out an act (ii) to benefit others (iii) without selfish motivations—as personal gains are an unintended by-product and not the goal of the prosocial act (Batson, 1987; Batson et al., 1981; Jensen, 2016). Previous research has suggested that these behaviors represent a broad and multidimensional construct constituted of cognitive and motivational processes (Coke et al., 1978; Padilla-Walker and Carlo, 2014).
Socio-cognitive abilities (e.g., mentalizing) are required for prosocial acts to understand another person’s needs, infer goals across variable and novel contexts, and recognize when to engage in helping behavior (Warneken, 2015). Humans support those who are in need and ask for help, and they are more likely to do so if the latter are friends or ingroup members (Abrams et al., 2015; Warneken and Tomasello, 2009b; Weller and Hansen Lagattuta, 2013; Young et al., 1999). Prosocial acts require these abilities because they presuppose representations of self- and other-related intentions and goals (Batson, 1991; Brownell et al., 2006; Smiley, 2002), and ontogenetic evidence indicates that the development of complex prosocial behaviors is concomitant with the refinement of mentalizing abilities (Abrams et al., 2015; Eisenberg et al., 2015; Warneken and Tomasello, 2009a).
Further, the motivation to help (e.g., empathic concern) is required to resonate with the other’s needy situation and to be motivated to see the other’s needs satisfied (Dovidio and Penner, 2007). Such motivation has been proposed to be an evolutionary outcome of empathy (de Waal, 2008d; Rumble et al., 2009; Xu et al., 2018). Humans exhibit empathic concerns about the welfare of others (Batson, 2011) and based on these concerns, they feel committed to alleviate others’ distress and pain (de Waal, 2008d; Warneken, 2015; Warneken and Tomasello, 2009a).
Building on this evidence, a qualitative review of the neuroimaging literature has proposed a set of brain regions that are likely involved in prosociality (Chakroff and Young, 2014). On the one hand, socio-cognitive abilities are instantiated in brain areas broadly associated with the mentalizing network (Bzdok et al., 2012) to support processes that lead to the recognition of another person’s needs and the circumstances in which prosocial behaviors are appropriate. Candidate regions involve brain areas previously implicated in social trait attributions and social event knowledge, such as the posterior cingulate cortex (PCC) and medial prefrontal cortex (mPFC) (Hackel et al., 2015; Krueger et al., 2009; Mitchell et al., 2009; Murray et al., 2012). On the other hand, the motivation for a prosocial act is instantiated in brain regions broadly associated with the empathy network (Bzdok et al., 2012; Fan et al., 2011) to support processes that lead to identifying oneself with another person’s needy situation and thus to the emergence of empathic concerns (Chakroff and Young, 2014). Brain regions like the middle cingulate cortex (MCC) and anterior insula (AI) might play a central role given their involvement in vicarious affective experiences (e.g., pain, disgust, and distress) that promote empathic concern (Corradi-Dell’Acqua et al., 2016; Fan et al., 2011).
One limitation of the current literature is that brain regions involved in prosociality have been inferred from task-based functional MRI (fMRI) investigations of single prosocial behaviors (Hackel et al., 2015; Karns et al., 2017; Moll et al., 2006; Park et al., 2017). Evidence of the common neural network underlying all these prosocial acts is still lacking. Further, small sample sizes and analytic flexibility (combined with publication bias) pertain to other concerns for individual fMRI studies (Feredoes and Postle, 2007; Raemaekers et al., 2007). Moreover, even though a recent comparative meta-analysis has provided preliminary evidence for the involvement of the mPFC in giving behaviors (Cutler and Campbell-Meiklejohn, 2019), it is still unclear to which extent the neural underpinnings of other prosocial behaviors are part of the mentalizing and empathy brain networks hypothesized to be involved in those very behaviors. Because prosociality is such a composite and multidimensional construct, a quantitative meta-analysis of the neuroimaging evidence on its components might be the most suitable means to unearth its neural underpinnings.
Here, we aimed at testing the presence of the above-mentioned cognitive and motivational modules of prosocial behaviors at the neural level and investigated whether there are brain patterns preferentially associated with prosociality as opposed to mentalizing and empathy. Aside from mentalizing and empathy brain areas, brain regions associated with action-outcome evaluations and action planning might be involved as well, as prosocial behaviors also require carrying out actions that help others. To this end, we performed a quantitative meta-analysis implementing the activation likelihood estimation (ALE) algorithm (Eickhoff et al., 2009) and meta-analytic connectivity analyses to identify the meta-analytic neural profile of prosociality, mentalizing, and empathy, and examined their convergences and divergences. Finally, to characterize the functions of the emerging neural patterns, we employed functional decoding (FD) analyses (Eickhoff et al., 2017).
Section snippets
Literature search and selection
In this work, we performed three meta-analyses to identify meta-analytic brain regions consistently engaged by (1) prosociality, (2) mentalizing, and (3) empathy. A systematic online database search was performed on PubMed and Google Scholar by entering various combinations of relevant search items referring to behaviors that the literature had identified as prosocial behaviors. The following keywords were used for the meta-analysis on prosociality: ‘generosity’, ‘altruism’, ‘cooperation’,
Meta-analytic clusters for prosociality, empathy and mentalizing
We first identified brain regions consistently activated by prosociality, empathy, and mentalizing. For prosociality, we searched both broad and general keywords, such as prosocial and prosocial behaviors, as well as more specific key terms describing single prosocial behaviors, such as generosity, altruism, charity, and donation. Moreover, to be able to include all appropriate and relevant behaviors, scientific paradigms known to experimentally investigate forms of prosocial behaviors were
Discussion
Prosocial behaviors refer to a wide range of acts aimed at benefitting others (e.g., helping, sharing, and caring). Psychological accounts posit that the psychological components of prosocial behaviors comprehend socio-cognitive abilities to understand the other’s goals, and empathic concern to be motivated to help. This hypothesis predicts the engagement of the mentalizing and empathy brain networks on the neural level. Here, we found partial evidence to support this hypothesis. In particular,
Author contribution
G.B. conceived the study idea. G.B. and F.K. designed the study. G.B. collected the data. G.B. and J.A.C. carried out the data analysis. S.B.E. provided analysis tools. G.B. wrote the manuscript with edits from F.K., J.A.C. and S.B.E.. All authors approved the final version of the manuscript.
Declaration of Competing Interest
The authors declare no conflicts of interest, financial or otherwise.
Acknowledgments
G.B. is supported by the Max Planck Society. S.B.E. is supported by the National Institute of Mental Health (R01-MH074457), the Helmholtz Portfolio Theme "Supercomputing and Modeling for the Human Brain" and the European Union’s Horizon 2020 Research and Innovation Programme under Grant Agreement No. 785907 (HBP SGA2). We finally would like to acknowledge the funding that has supported the enhanced NKI-RS project, from which the resting-state data were obtained (NIMH BRAINS R01MH094639-01).
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