Encoding of Vicarious Reward Prediction in Anterior Cingulate Cortex and Relationship with Trait Empathy

Lockwood, Patricia L.; Apps, Matthew A. J.; Roiser, Jonathan P.; Viding, Essi

doi:10.1523/jneurosci.1703-15.2015

Cited by 107 publications

(148 citation statements)

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“…This may seem surprising given that these regions have previously been implicated in empathy and/or social behavior (15,29,30,37). Although it is difficult to interpret a null finding, because there can be a number of reasons that a particular neural response is not observed, we note that in this experiment, participants were performing their task in a different reference frame (see refs.…”

Section: Discussionmentioning

confidence: 84%

“…Empathy, the capacity to vicariously experience and understand the affect of others (23)(24)(25)(26)(27), has been hypothesized to be a critical motivator of prosocial behaviors (25)(26)(27)(28). Previous studies have consistently shown that empathy can modulate neural responses to viewing others' pain (29) and viewing desirable outcomes (rewards) that will be delivered to others (15,30). Moreover, although empathy can be broken down into separable components associated with different social behaviors and traits (23,31,32), studies have suggested that both cognitive and affective aspects of empathic processing may motivate prosocial behaviors (33).…”

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confidence: 99%

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Neurocomputational mechanisms of prosocial learning and links to empathy

Lockwood

Apps

Valton

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Reinforcement learning theory powerfully characterizes how we learn to benefit ourselves. In this theory, prediction errors-the difference between a predicted and actual outcome of a choice-drive learning. However, we do not operate in a social vacuum. To behave prosocially we must learn the consequences of our actions for other people. Empathy, the ability to vicariously experience and understand the affect of others, is hypothesized to be a critical facilitator of prosocial behaviors, but the link between empathy and prosocial behavior is still unclear. During functional magnetic resonance imaging (fMRI) participants chose between different stimuli that were probabilistically associated with rewards for themselves (self), another person (prosocial), or no one (control). Using computational modeling, we show that people can learn to obtain rewards for others but do so more slowly than when learning to obtain rewards for themselves. fMRI revealed that activity in a posterior portion of the subgenual anterior cingulate cortex/basal forebrain (sgACC) drives learning only when we are acting in a prosocial context and signals a prosocial prediction error conforming to classical principles of reinforcement learning theory. However, there is also substantial variability in the neural and behavioral efficiency of prosocial learning, which is predicted by trait empathy. More empathic people learn more quickly when benefitting others, and their sgACC response is the most selective for prosocial learning. We thus reveal a computational mechanism driving prosocial learning in humans. This framework could provide insights into atypical prosocial behavior in those with disorders of social cognition.reinforcement learning theory | prosocial behavior | empathy | reward | subgenual anterior cingulate cortex P rosocial behaviors, namely, social behaviors or actions intended to benefit others, are a fundamental but poorly understood aspect of social interaction (1). To behave prosocially, animals need to learn about the consequences that their actions can have for others. In reinforcement learning theory (RLT), prediction errors (PEs)-differences between expected and actual outcomesdrive learning (2). RLT provides a powerful framework for understanding how animals learn to obtain rewards for themselves (3). However, the processes by which animals learn to make choices that benefit others are unknown. Here we use RLT to characterize prosocial learning, combining functional magnetic resonance imaging (fMRI) and detailed computational modeling of behavior.Studies using economic games, moral judgments, or charity donation tasks have consistently reported activity in the ventral striatum, posterior regions of the subgenual cingulate cortex/basal forebrain (hereinafter referred to as sgACC), dorsal anterior cingulate cortex (dACC), and dorsolateral prefrontal cortex (DLPFC) during prosocial behavior (4-7). Each of these regions receives input from midbrain dopaminergic neurons (8), and these cortical regions all project to the ventral ...

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Section: Discussionmentioning

confidence: 84%

mentioning

confidence: 99%

Neurocomputational mechanisms of prosocial learning and links to empathy

Lockwood

Apps

Valton

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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182

236

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“…However, there is evidence that the VMPFC and DMPFC regions differentially code between fair and unfair offers, including in studies where the magnitudes of offers to self and other were controlled for [see (Feng et al., 2015) for a meta‐analysis]. Studies that have directly compared activity to the same magnitude of rewards being delivered to self and other, find that activity in the VMPFC and DMPFC is not different between self and other rewards (Apps & Ramnani, 2014; Lockwood et al., 2015; Yoshida, Saito, Iriki, & Isoda, 2012). If activity in these regions is equally sensitive to payoffs to self and other, but is different to when these monetary values are unfairly divided, it suggests that the response in these regions is sensitive to the fairness of offers.…”

Section: Discussionmentioning

confidence: 99%

“…This includes evidence that the ACCg is sensitive to the predicted value of a reward another will receive, and also to the decisions others make about rewards, as well as the offers others make to us during the UG (Apps & Ramnani, 2014; Apps et al., 2015; Gabay et al., 2014; Lockwood et al., 2015). Whilst the design of this experiment was not optimized to look at how the brain processes the rewards received by others, the ACCg did respond differently to ingroup individuals compared to others.…”

Section: Discussionmentioning

confidence: 99%

“…Research across species has highlighted three subregions of the medial prefrontal cortex (mPFC) that each play an important role in processing social information (Amodio & Frith, 2006); the ventromedial portions of the PFC (VMPFC; area 32), dorso‐medial PFC (DMPFC; areas 8 and 9 on the medial surface of the superior frontal gyrus), and portions of the anterior cingulate cortex (ACC; particularly areas 24a/b lying in the gyrus) (Apps, Lesage, & Ramnani, 2015; Apps, Rushworth, & Chang, 2016; Cooper, Kreps, Wiebe, Pirkl, & Knutson, 2010; Frith & Frith, 2006; Hare, Camerer, Knoepfle, & Rangel, 2010; Haroush & Williams, 2015; Lee, 2008; Lee & Seo, 2016; Lockwood, Apps, Roiser, & Viding, 2015). Lesions to these regions impair and reduce the execution of social behaviors and can lead to the inability to adhere to group or social norms (Anderson, Bechara, Damasio, Tranel, & Damasio, 1999; Gu et al., 2015; Hadland, Rushworth, Gaffan, & Passingham, 2003; Rudebeck, Buckley, Walton, & Rushworth, 2006; Tranel, Bechara, & Denburg, 2002).…”

Section: Introductionmentioning

confidence: 99%

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Not on my team: Medial prefrontal cortex responses to ingroup fusion and unfair monetary divisions

et al. 2018

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ObjectivePeople are highly attuned to fairness, with people willingly suffering personal costs to prevent others benefitting from unfair acts. Are fairness judgments influenced by group alignments? A new theory posits that we favor ingroups and denigrate members of rival outgroups when our personal identity is fused to a group. Although the mPFC has been separately implicated in group membership and fairness processing, it is unclear whether group alignments affect medial prefrontal cortex (mPFC) activity in response to fairness. Here, we examine the contribution of different regions of the mPFC to processing from ingroup and outgroup members and test whether its response differs depending on how fused we are to an ingroup.MethodsSubjects performed rounds of the Ultimatum Game, being offered fair or unfair divisions of money from supporters of the same soccer team (ingroup), the fiercest rival (outgroup) or neutral individuals whilst undergoing functional Magnetic Resonance Imaging (fMRI).ResultsStrikingly, people willingly suffered personal costs to prevent outgroup members benefitting from both unfair and fair offers. Activity across dorsal and ventral (VMPFC) portions of the mPFC reflected an interaction between fairness and group membership. VMPFC activity in particular was consistent with it coding one's fusion to a group, with the fairness by group membership interaction correlating with the extent that the responder's identity was fused to the ingroup.ConclusionsThe influence of fusion on social behavior therefore seems to be linked to processing in the VMPFC.

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Psychopathy, Diminished Capacity and Responsibility

Nair

Weinstock

The International Handbook of Psychopathic Disorders and the Law

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Encoding of Vicarious Reward Prediction in Anterior Cingulate Cortex and Relationship with Trait Empathy

Cited by 107 publications

References 45 publications

Neurocomputational mechanisms of prosocial learning and links to empathy

Neurocomputational mechanisms of prosocial learning and links to empathy

Not on my team: Medial prefrontal cortex responses to ingroup fusion and unfair monetary divisions

Psychopathy, Diminished Capacity and Responsibility

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