Neuronal reference frames for social decisions in primate frontal cortex

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112

Despite the importance of valuing another person's welfare for prosocial behavior, currently we have only a limited understanding of how these values are represented in the brain and, more importantly, how they give rise to individual variability in prosociality. In the present study, participants underwent functional magnetic resonance imaging while performing a prosocial learning task in which they could choose to benefit themselves and/or another person. Choice behavior indicated that participants valued the welfare of another person, although less so than they valued their own welfare. Neural data revealed a spatial gradient in activity within the medial prefrontal cortex (MPFC), such that ventral parts predominantly represented self-regarding values and dorsal parts predominantly represented other-regarding values. Importantly, compared with selfish individuals, prosocial individuals showed a more gradual transition from selfregarding to other-regarding value signals in the MPFC and stronger MPFC-striatum coupling when they made choices for another person rather than for themselves. The present study provides evidence of neural markers reflecting individual differences in human prosociality.R anging from small acts of kindness in daily life to self-sacrificing altruism under life-threatening situations, we often observe large individual differences in how humans value another person's welfare. This differential valuation process seems to be the key to understanding various human prosocial behaviors, which are fundamental to the sustainability of human society (1). The underlying neural mechanisms and their relationship to individual differences in prosociality remain unclear, however.Perhaps the most powerful way of assessing how an outcome is valued is to use an instrumental learning paradigm that examines whether the occurrence of a response increases when it is followed by that outcome (2). The mechanisms underlying this type of learning have been described more formally with a computational model, known as the advantage learning model (3-5), which has been used successfully to reveal the neuroanatomical substrates of subjective valuation (3,4,6). Previous research has further refined the neurobiological model of reinforcement learning by emphasizing the specific roles played by the medial frontal cortex and the striatum; the medial frontal cortex computes the value of the chosen action, whereas the striatum processes reward prediction errors during reinforcement learning (4, 6-10).Unlike our current understanding of the valuation process for self-regarding choices (3, 6-12), it is much less clear whether learning also can be driven by other-regarding values, and whether this other-regarding valuation relies on the same mechanisms of reinforcement learning as those used for self. Moreover, despite the rapidly accumulating research on reward processing in social domains (13-19), the question remains of how neural representation of self-regarding vs. other-regarding values is related to individual differen...

supporting

confidence: 77%

Spatial gradient in value representation along the medial prefrontal cortex reflects individual differences in prosociality

Sul

Tobler

Hein

et al. 2015

127

112

“…The two models of most interest were Y = β 0 + β 1 A + β 2 W + β 4 AW + e; [2] which tests neuronal coding of actor for own reward, and Y = β 0 + β 1 A + β 3 Z + β 5 AZ + e; [3] which tests neuronal coding of actor for conspecific's reward. We also included a model that tests coding of reward only Y = β 0 + β 2 W + β 3 Z + e: [4] All models implied by the unrestricted model (Eq. 1), as well as the temporal discounting and action cost models, are detailed in Eqs.…”

Section: Eye Movement Analysismentioning

confidence: 99%

“…Recent evidence suggests separate coding of social reward and action in the neuronal activity of distinct frontal cortical areas of monkeys. Reward neurons distinguish between own and other's reward (3,4) and show differential activity during social competition (5) and movement (6). Action neurons respond to the observation of movement of social partners (7), differentiate between own and other's movements (8), and detect other's error commission (9).…”

mentioning

confidence: 99%

Activity of striatal neurons reflects social action and own reward

Báez-Mendoza

Harris

Schultz

2013

Social interactions provide agents with the opportunity to earn higher benefits than when acting alone and contribute to evolutionary stable strategies. A basic requirement for engaging in beneficial social interactions is to recognize the actor whose movement results in reward. Despite the recent interest in the neural basis of social interactions, the neurophysiological mechanisms identifying the actor in social reward situations are unknown. A brain structure well suited for exploring this issue is the striatum, which plays a role in movement, reward, and goal-directed behavior. In humans, the striatum is involved in social processes related to reward inequity, donations to charity, and observational learning. We studied the neurophysiology of social action for reward in rhesus monkeys performing a reward-giving task. The behavioral data showed that the animals distinguished between their own and the conspecific's reward and knew which individual acted. Striatal neurons coded primarily own reward but rarely other's reward. Importantly, the activations occurred preferentially, and in approximately similar fractions, when either the own or the conspecific's action was followed by own reward. Other striatal neurons showed social action coding without reward. Some of the social action coding disappeared when the conspecific's role was simulated by a computer, confirming a social rather than observational relationship. These findings demonstrate a role of striatal neurons in identifying the social actor and own reward in a social setting. These processes may provide basic building blocks underlying the brain's function in social interactions.

“…How social and nonsocial signals in these circuits are integrated to mediate decisions with respect to others remains imperfectly understood, in part, due to the indirect nature of hemodynamic signals measured in human neuroimaging experiments that constitute the bulk of this research. Recent advances in the development of neurophysiological and neuropharmacological models of social decision-making, however, permit more direct inquiry into the neural mechanisms mediating other-regarding behavior (7)(8)(9)(10)(11).…”

mentioning

confidence: 99%

Neural mechanisms of social decision-making in the primate amygdala

Chang

Fagan

Toda

et al. 2015

134

117

Social decisions require evaluation of costs and benefits to oneself and others. Long associated with emotion and vigilance, the amygdala has recently been implicated in both decision-making and social behavior. The amygdala signals reward and punishment, as well as facial expressions and the gaze of others. Amygdala damage impairs social interactions, and the social neuropeptide oxytocin (OT) influences human social decisions, in part, by altering amygdala function. Here we show in monkeys playing a modified dictator game, in which one individual can donate or withhold rewards from another, that basolateral amygdala (BLA) neurons signaled social preferences both across trials and across days. BLA neurons mirrored the value of rewards delivered to self and others when monkeys were free to choose but not when the computer made choices for them. We also found that focal infusion of OT unilaterally into BLA weakly but significantly increased both the frequency of prosocial decisions and attention to recipients for context-specific prosocial decisions, endorsing the hypothesis that OT regulates social behavior, in part, via amygdala neuromodulation. Our findings demonstrate both neurophysiological and neuroendocrinological connections between primate amygdala and social decisions.amygdala | social decision | value mirroring | oxytocin | hierarchical modeling H ow we treat others impacts not only their well-being but our own. Human society depends on cooperation, charity, and altruism, as well as institutions to regulate selfish biases. In humans, these behaviors involve perspective-taking, empathy, and theory of mind (1, 2), and the rudiments of these capacities appear to mediate complex social behavior in animals (3). Recent research has sketched a rough outline of the neural circuits that contribute to complex social behavior (4, 5). These comprise a set of domaingeneral brain areas, including the ventromedial prefrontal cortex and ventral striatum, that process information about reward and punishment and contribute to decision-making, and a set of specialized areas, including the temporoparietal junction and medial prefrontal cortex, that process specifically social information (4, 6). How social and nonsocial signals in these circuits are integrated to mediate decisions with respect to others remains imperfectly understood, in part, due to the indirect nature of hemodynamic signals measured in human neuroimaging experiments that constitute the bulk of this research. Recent advances in the development of neurophysiological and neuropharmacological models of social decision-making, however, permit more direct inquiry into the neural mechanisms mediating other-regarding behavior (7-11).The amygdala, especially the basolateral division (BLA), has been implicated in both decision-making and social perception, inviting the possibility that it contributes to decision-making with respect to others (12)(13)(14)(15)(16)(17). This set of nuclei is well known for contributions to emotional experience and expression, especia...