Mapping social reward and punishment processing in the human brain: A voxel-based meta-analysis of neuroimaging findings using the Social Incentive Delay task

Abstract

Highlights• Voxel-based meta-analysis of the neural underpinnings of social incentive processing • We map the brain regions involved in the processing of social incentives in humans • We identify new regions missed in individual studies as a result of lack of power • Our work can inform research on pathological brain processing of social incentives ABSTRACT Social incentives (rewards or punishments) motivate human learning and behaviour, and alterations in the brain circuits involved in the processing social incentives have been linked with several neuropsychiatric disorders.However, questions still remain about the exact neural substrates implicated in social incentive processing. Here, we conducted four Anisotropic Effect Size Signed Differential Mapping voxel-based meta-analyses of fMRI studies investigating the neural correlates of the anticipation and receipt of social rewards and punishments using the Social Incentive Delay task. We map the regions involved in each of these four processes in the human brain, identify decreases in the BOLD signal during the anticipation of both social reward and punishment avoidance that were missed in individual studies due to a lack of power, and characterise the effect size and direction of changes in the BOLD signal for each brain area. Our results provide a better understanding of the brain circuitry involved in social incentive processing and can inform hypotheses about potentially disrupted brain areas linked with dysfunctional social incentive processing during disease.

Default Mode Network spatial configuration varies across task domains

“…To the best of our knowledge, deception tasks were not previously related to the network, although the social nature of such paradigms likely justifies this result. Similarly, we are not aware of many explicit links between reward functions and DMN in the literature (Martins et al, 2021), albeit there is strong evidence to associate the mPFC to such mechanisms (Hiser and Koenigs, 2018; Lieberman et al, 2019; Schneider and Koenigs, 2017; Xue et al, 2009). Interestingly, reasoning and problem-solving paradigms had a significant effect on the CAREN mask (Doucet et al, 2019), suggesting that the DMN might then play a role outside of what is considered internal mentation in the strictest sense.…”

“…This is mostly due to a large amount of foci covering the whole mPFC. The latter is known to modulate reward mechanisms (Ferenczi et al, 2016), to respond to the outcome of risky decisions (Xue et al, 2009), and to activate when receiving a social reward (Martins et al, 2021). Reward mechanisms could be considered as an example of functions meant to monitor internal states, yet crucial for the implementation of behavior.…”

“…Since those observations, many further functions were shown to be associated to this network. Other than self-referential and emotional processes (Buckner and Carroll, 2007; D’Argembeau et al, 2010; Denny et al, 2012; Engen et al, 2017; Fingelkurts et al, 2020; Fossati et al, 2003; Knyazev et al, 2020; Molnar-Szakacs and Uddin, 2013; Northoff et al, 2006; Northoff and Bermpohl, 2004; Ochsner et al, 2005, 2004; Satpute and Lindquist, 2019; Uddin et al, 2007), the DMN turned out to be related to memory and mental time-travel (Addis et al, 2007; Cabeza et al, 1997; Foster et al, 2012; Kim, 2016; Murphy et al, 2018; Rugg and Vilberg, 2013; Schacter et al, 2008, 2007; Spreng et al, 2015; Svoboda et al, 2006; Yang et al, 2013), mental simulation and scene construction (Gerlach et al, 2011; Hassabis et al, 2007; Hassabis and Maguire, 2007; Spreng and Grady, 2010), theory of mind (ToM) and social cognition (Amft et al, 2015; Mar, 2011; Mars et al, 2012; Mwilambwe-Tshilobo and Spreng, 2021; Rilling et al, 2004; Ruby and Decety, 2004; Saxe and Kanwisher, 2003; Saxe and Powell, 2006; Spreng and Andrews-Hanna, 2015), moral judgment (Bzdok et al, 2012; Greene et al, 2001; Harrison et al, 2008; Pujol et al, 2008), semantic processing (Binder et al, 1999, 2009; Chiou et al, 2020; Evans et al, 2020; Lanzoni et al, 2020), and reward mechanisms (Lopez-Persem et al, 2020; Martins et al, 2021; Xue et al, 2009). However, most of these psychological functions can still be somewhat associated with the resting state (Wen et al, 2020).…”

No support for oxytocin modulation of reward-related brain function in autism: evidence from a randomized controlled trial

“…Because of methodological similarities, one might expect the results from the current study to be in line with results from the first study using the incentive delay task. However, even though the monetary or social incentive delay task is one of the most often used tasks to examine reward processing [77], several variations exist that may influence the magnitude of potential oxytocin effects. For example, the choice of stimuli (showing the amount of money won in numbers [48] vs. pictures of money, smiling vs. laughing faces) could influence the perceived value of the rewards and the subjective relevance of the task.…”

“…To increase the sensitivity of our analyses, we first examined all effects in a priori defined regions of interest (ROI), which were defined separately for the anticipation and outcome phases. The ventral striatum was chosen as region of interest for the anticipation phase due to its pivotal role in reward processing, especially during the anticipation of rewards [51,76,77]. The bilateral ventral striatum mask consisted of two 8 mm spheres around peak coordinates (MNI coordinates left: −10, 10, −2; right: 12, 14, −4) from a meta-analysis of ventral striatum activation associated with reward anticipation [78].…”