Neural Mechanisms of Social Cognition in Primates.

Activity in a network of areas spanning the superior temporal sulcus, dorsomedial frontal cortex, and anterior cingulate cortex is concerned with how nonhuman primates negotiate the social worlds in which they live. Central aspects of these circuits are retained in humans. Activity in these areas codes for primates' interactions with one another, their attempts to find out about one another, and their attempts to prevent others from finding out too much about themselves. Moreover, important features of the social world, such as dominance status, cooperation, and competition, modulate activity in these areas. We consider the degree to which activity in these regions is simply encoding an individual's own actions and choices or whether this activity is especially and specifically concerned with social cognition. Recent advances in comparative anatomy and computational modeling may help us to gain deeper insights into the nature and boundaries of primate social cognition.

Local and global reward learning in the lateral frontal cortex show differential development during human adolescence.

Reward-guided choice is fundamental for adaptive behaviour and depends on several component processes supported by prefrontal cortex. Here, across three studies, we show that two such component processes, linking reward to specific choices and estimating the global reward state, develop during human adolescence and are linked to the lateral portions of the prefrontal cortex. These processes reflect the assignment of rewards contingently to local choices, or noncontingently, to choices that make up the global reward history. Using matched experimental tasks and analysis platforms, we show the influence of both mechanisms increase during adolescence (study 1) and that lesions to lateral frontal cortex (that included and/or disconnected both orbitofrontal and insula cortex) in human adult patients (study 2) and macaque monkeys (study 3) impair both local and global reward learning. Developmental effects were distinguishable from the influence of a decision bias on choice behaviour, known to depend on medial prefrontal cortex. Differences in local and global assignments of reward to choices across adolescence, in the context of delayed grey matter maturation of the lateral orbitofrontal and anterior insula cortex, may underlie changes in adaptive behaviour.

A neuroscientific perspective on the computational theory of social groups.

We welcome a computational theory on social groups, yet we argue it would benefit from a broader scope. A neuroscientific perspective offers the possibility to disentangle which computations employed in a group context are genuinely social in nature. Concurrently, we emphasize that a unifying theory of social groups needs to additionally consider higher-level processes like motivations and emotions.

The Good, the Bad, and the Irrelevant: Neural Mechanisms of Learning Real and Hypothetical Rewards and Effort.

Natural environments are complex, and a single choice can lead to multiple outcomes. Agents should learn which outcomes are due to their choices and therefore relevant for future decisions and which are stochastic in ways common to all choices and therefore irrelevant for future decisions between options. We designed an experiment in which human participants learned the varying reward and effort magnitudes of two options and repeatedly chose between them. The reward associated with a choice was randomly real or hypothetical (i.e., participants only sometimes received the reward magnitude associated with the chosen option). The real/hypothetical nature of the reward on any one trial was, however, irrelevant for learning the longer-term values of the choices, and participants ought to have only focused on the informational content of the outcome and disregarded whether it was a real or hypothetical reward. However, we found that participants showed an irrational choice bias, preferring choices that had previously led, by chance, to a real reward in the last trial. Amygdala and ventromedial prefrontal activity was related to the way in which participants' choices were biased by real reward receipt. By contrast, activity in dorsal anterior cingulate cortex, frontal operculum/anterior insula, and especially lateral anterior prefrontal cortex was related to the degree to which participants resisted this bias and chose effectively in a manner guided by aspects of outcomes that had real and more sustained relationships with particular choices, suppressing irrelevant reward information for more optimal learning and decision making. SIGNIFICANCE STATEMENT: In complex natural environments, a single choice can lead to multiple outcomes. Human agents should only learn from outcomes that are due to their choices, not from outcomes without such a relationship. We designed an experiment to measure learning about reward and effort magnitudes in an environment in which other features of the outcome were random and had no relationship with choice. We found that, although people could learn about reward magnitudes, they nevertheless were irrationally biased toward repeating certain choices as a function of the presence or absence of random reward features. Activity in different brain regions in the prefrontal cortex either reflected the bias or reflected resistance to the bias.

Neural activity tracking identity and confidence in social information.

Humans learn about the environment either directly by interacting with it or indirectly by seeking information about it from social sources such as conspecifics. The degree of confidence in the information obtained through either route should determine the impact that it has on adapting and changing behaviour. We examined whether and how behavioural and neural computations differ during non-social learning as opposed to learning from social sources. Trial-wise confidence judgements about non-social and social information sources offered a window into this learning process. Despite matching exactly the statistical features of social and non-social conditions, confidence judgements were more accurate and less changeable when they were made about social as opposed to non-social information sources. In addition to subjective reports of confidence, differences were also apparent in the Bayesian estimates of participants' subjective beliefs. Univariate activity in dorsomedial prefrontal cortex and posterior temporoparietal junction more closely tracked confidence about social as opposed to non-social information sources. In addition, the multivariate patterns of activity in the same areas encoded identities of social information sources compared to non-social information sources.

People's decisions are influenced by their beliefs, which may be based on advice from other humans or, alternatively, on information from non-human sources such as road signs. But which sources do we find more reliable? Although scientists have studied the importance of social context in the way we process information, it is not fully understood how the brain processes information differently depending on who provides it. Trudel et al. investigated the differences in the way humans evaluate information from human sources, such as advisors, compared to non-human sources, like inanimate objects, by monitoring brain activity and analyzing the results using a computational approach. In the experiments, 24 participants received a reward for locating a hidden dot on a circle under two different conditions: they either received a clue on the dot's location from an image of a human face (social condition), representing an advisor, or from an inanimate object (non-social condition). Participants received information from many different advisors and inanimate objects, and the accuracy of the clues given by any of them varied from source to source. Each time, participants reported whether they thought the advice was reliable. The results of monitoring the participants' brain activity showed that they used different strategies when assessing the reliability of advice from a human than when the information came from a non-human source. Additionally, participants based their judgments about an advisor more strongly on past experiences with them, that is, if an advisor had given them good advice in the past, they were more likely to rely on their advice. Conversely, judgments about an inanimate object were based more strongly on recent experiences with that object. Interestingly, participants were more certain when making judgments about the accuracy of cues given by advisors compared to inanimate objects, and they also updated their assessment of human sources less according to new evidence that contradicted their initial belief. This suggests that people may form more stable opinions about the reliability of sources when they receive information in social contexts, possibly because they expect more consistent behavior from humans. This stability in judgments about advisors was also reflected in the signal of brain areas that are often involved when interacting with others. The work of Trudel et al. shows that even the suggestion that the source of a piece of advice is human can change how we process the information. This is especially important because humans spend increasingly more time in the digital world. Awareness of our biased assessment of human sources will have implications for designing interactive tools to guide human decision-making as well as strategies to develop critical thinking.

Distinct neural representations for prosocial and self-benefiting effort.

Prosocial behaviors-actions that benefit others-are central to individual and societal well-being. Although the mechanisms underlying the financial and moral costs of prosocial behaviors are increasingly understood, this work has often ignored a key influence on behavior: effort. Many prosocial acts are effortful, and people are averse to the costs of exerting them. However, how the brain encodes effort costs when actions benefit others is unknown. During fMRI, participants completed a decision-making task where they chose in each trial whether to "work" and exert force (30%-70% of maximum grip strength) or "rest" (no effort) for rewards (2-10 credits). Crucially, on separate trials, they made these decisions either to benefit another person or themselves. We used a combination of multivariate representational similarity analysis and model-based univariate analysis to reveal how the costs of prosocial and self-benefiting efforts are processed. Strikingly, we identified a unique neural signature of effort in the anterior cingulate gyrus (ACCg) for prosocial acts, both when choosing to help others and when exerting force to benefit them. This pattern was absent for self-benefiting behaviors. Moreover, stronger, specific representations of prosocial effort in the ACCg were linked to higher levels of empathy and higher subsequent exerted force to benefit others. In contrast, the ventral tegmental area and ventral insula represented value preferentially when choosing for oneself and not for prosocial acts. These findings advance our understanding of the neural mechanisms of prosocial behavior, highlighting the critical role that effort has in the brain circuits that guide helping others.

Polarity of uncertainty representation during exploration and exploitation in ventromedial prefrontal cortex.

Environments furnish multiple information sources for making predictions about future events. Here we use behavioural modelling and functional magnetic resonance imaging to describe how humans select predictors that might be most relevant. First, during early encounters with potential predictors, participants' selections were explorative and directed towards subjectively uncertain predictors (positive uncertainty effect). This was particularly the case when many future opportunities remained to exploit knowledge gained. Then, preferences for accurate predictors increased over time, while uncertain predictors were avoided (negative uncertainty effect). The behavioural transition from positive to negative uncertainty-driven selections was accompanied by changes in the representations of belief uncertainty in ventromedial prefrontal cortex (vmPFC). The polarity of uncertainty representations (positive or negative encoding of uncertainty) changed between exploration and exploitation periods. Moreover, the two periods were separated by a third transitional period in which beliefs about predictors' accuracy predominated. The vmPFC signals a multiplicity of decision variables, the strength and polarity of which vary with behavioural context.

Causal manipulation of self-other mergence in the dorsomedial prefrontal cortex.

To navigate social environments, people must simultaneously hold representations about their own and others' abilities. During self-other mergence, people estimate others' abilities not only on the basis of the others' past performance, but the estimates are also influenced by their own performance. For example, if we perform well, we overestimate the abilities of those with whom we are co-operating and underestimate competitors. Self-other mergence is associated with specific activity patterns in the dorsomedial prefrontal cortex (dmPFC). Using a combination of non-invasive brain stimulation, functional magnetic resonance imaging, and computational modeling, we show that dmPFC neurostimulation silences these neural signatures of self-other mergence in relation to estimation of others' abilities. In consequence, self-other mergence behavior increases, and our assessments of our own performance are projected increasingly onto other people. This suggests an inherent tendency to form interdependent social representations and a causal role of the dmPFC in separating self and other representations.

Ageing is associated with disrupted reinforcement learning whilst learning to help others is preserved.

Reinforcement learning is a fundamental mechanism displayed by many species. However, adaptive behaviour depends not only on learning about actions and outcomes that affect ourselves, but also those that affect others. Using computational reinforcement learning models, we tested whether young (age 18-36) and older (age 60-80, total n = 152) adults learn to gain rewards for themselves, another person (prosocial), or neither individual (control). Detailed model comparison showed that a model with separate learning rates for each recipient best explained behaviour. Young adults learned faster when their actions benefitted themselves, compared to others. Compared to young adults, older adults showed reduced self-relevant learning rates but preserved prosocial learning. Moreover, levels of subclinical self-reported psychopathic traits (including lack of concern for others) were lower in older adults and the core affective-interpersonal component of this measure negatively correlated with prosocial learning. These findings suggest learning to benefit others is preserved across the lifespan with implications for reinforcement learning and theories of healthy ageing.

Identification and disruption of a neural mechanism for accumulating prospective metacognitive information prior to decision-making.

More than one type of probability must be considered when making decisions. It is as necessary to know one's chance of performing choices correctly as it is to know the chances that desired outcomes will follow choices. We refer to these two choice contingencies as internal and external probability. Neural activity across many frontal and parietal areas reflected internal and external probabilities in a similar manner during decision-making. However, neural recording and manipulation approaches suggest that one area, the anterior lateral prefrontal cortex (alPFC), is highly specialized for making prospective, metacognitive judgments on the basis of internal probability; it is essential for knowing which decisions to tackle, given its assessment of how well they will be performed. Its activity predicted prospective metacognitive judgments, and individual variation in activity predicted individual variation in metacognitive judgments. Its disruption altered metacognitive judgments, leading participants to tackle perceptual decisions they were likely to fail.

Ultrasound modulation of macaque prefrontal cortex selectively alters credit assignment-related activity and behavior.

Credit assignment is the association of specific instances of reward to the specific events, such as a particular choice, that caused them. Without credit assignment, choice values reflect an approximate estimate of how good the environment was when the choice was made­the global reward state­rather than exactly which outcome the choice caused. Combined transcranial ultrasound stimulation (TUS) and functional magnetic resonance imaging in macaques demonstrate credit assignment­related activity in prefrontal area 47/12o, and when this signal was disrupted with TUS, choice value representations across the brain were impaired. As a consequence, behavior was no longer guided by choice value, and decision-making was poorer. By contrast, global reward state­related activity in the adjacent anterior insula remained intact and determined decision-making after prefrontal disruption.

Global reward state affects learning and activity in raphe nucleus and anterior insula in monkeys.

People and other animals learn the values of choices by observing the contingencies between them and their outcomes. However, decisions are not guided by choice-linked reward associations alone; macaques also maintain a memory of the general, average reward rate - the global reward state - in an environment. Remarkably, global reward state affects the way that each choice outcome is valued and influences future decisions so that the impact of both choice success and failure is different in rich and poor environments. Successful choices are more likely to be repeated but this is especially the case in rich environments. Unsuccessful choices are more likely to be abandoned but this is especially likely in poor environments. Functional magnetic resonance imaging (fMRI) revealed two distinct patterns of activity, one in anterior insula and one in the dorsal raphe nucleus, that track global reward state as well as specific outcome events.

Multiple associative structures created by reinforcement and incidental statistical learning mechanisms.

Learning the structure of the world can be driven by reinforcement but also occurs incidentally through experience. Reinforcement learning theory has provided insight into how prediction errors drive updates in beliefs but less attention has been paid to the knowledge resulting from such learning. Here we contrast associative structures formed through reinforcement and experience of task statistics. BOLD neuroimaging in human volunteers demonstrates rigid representations of rewarded sequences in temporal pole and posterior orbito-frontal cortex, which are constructed backwards from reward. By contrast, medial prefrontal cortex and a hippocampal-amygdala border region carry reward-related knowledge but also flexible statistical knowledge of the currently relevant task model. Intriguingly, ventral striatum encodes prediction error responses but not the full RL- or statistically derived task knowledge. In summary, representations of task knowledge are derived via multiple learning processes operating at different time scales that are associated with partially overlapping and partially specialized anatomical regions.

Ventral anterior cingulate cortex and social decision-making.

Studies in the field of social neuroscience have recently made use of computational models of decision-making to provide new insights into how we learn about the self and others during social interactions. Importantly, these studies have increasingly drawn attention to brain areas outside of classical cortical "social brain" regions that may be critical for social processing. In particular, two portions of the ventral anterior cingulate cortex (vACC), subgenual anterior cingulate cortex and perigenual anterior cingulate cortex, have been linked to social and self learning signals, respectively. Here we discuss the emerging parallels between these studies. Uncovering the function of vACC during social interactions could provide important new avenues to understand social decision-making in health and disease.

Neural mechanisms for learning self and other ownership.

Sense of ownership is a ubiquitous and fundamental aspect of human cognition. Here we used model-based functional magnetic resonance imaging and a novel minimal ownership paradigm to probe the behavioural and neural mechanisms underpinning ownership acquisition for ourselves, friends and strangers. We find a self-ownership bias at multiple levels of behaviour from initial preferences to reaction times and computational learning rates. Ventromedial prefrontal cortex (vmPFC) and anterior cingulate sulcus (ACCs) responded more to self vs. stranger associations, but despite a pervasive neural bias to track self-ownership, no brain area tracked self-ownership exclusively. However, ACC gyrus (ACCg) specifically coded ownership prediction errors for strangers and ownership associative strength for friends and strangers but not for self. Core neural mechanisms for associative learning are biased to learn in reference to self but also engaged when learning in reference to others. In contrast, ACC gyrus exhibits specialization for learning about others.

Simultaneous representation of a spectrum of dynamically changing value estimates during decision making.

Decisions are based on value expectations derived from experience. We show that dorsal anterior cingulate cortex and three other brain regions hold multiple representations of choice value based on different timescales of experience organized in terms of systematic gradients across the cortex. Some parts of each area represent value estimates based on recent reward experience while others represent value estimates based on experience over the longer term. The value estimates within these areas interact with one another according to their temporal scaling. Some aspects of the representations change dynamically as the environment changes. The spectrum of value estimates may act as a flexible selection mechanism for combining experience-derived value information with other aspects of value to allow flexible and adaptive decisions in changing environments.

Inverted activity patterns in ventromedial prefrontal cortex during value-guided decision-making in a less-is-more task.

Ventromedial prefrontal cortex has been linked to choice evaluation and decision-making in humans but understanding the role it plays is complicated by the fact that little is known about the corresponding area of the macaque brain. We recorded activity in macaques using functional magnetic resonance imaging during two very different value-guided decision-making tasks. In both cases ventromedial prefrontal cortex activity reflected subjective choice values during decision-making just as in humans but the relationship between the blood oxygen level-dependent signal and both decision-making and choice value was inverted and opposite to the relationship seen in humans. In order to test whether the ventromedial prefrontal cortex activity related to choice values is important for decision-making we conducted an additional lesion experiment; lesions that included the same ventromedial prefrontal cortex region disrupted normal subjective evaluation of choices during decision-making.

Self-Other Mergence in the Frontal Cortex during Cooperation and Competition.

To survive, humans must estimate their own ability and the abilities of others. We found that, although people estimated their abilities on the basis of their own performance in a rational manner, their estimates of themselves were partly merged with the performance of others. Reciprocally, their ability estimates for others also reflected their own, as well as the others', performance. Self-other mergence operated in a context-dependent manner: interacting with high or low performers, respectively, enhanced and diminished own ability estimates in cooperative contexts, but the opposite occurred in competitive contexts. Self-other mergence not only influenced subjective evaluations, it also affected how people subsequently objectively adjusted their performance. Perigenual anterior cingulate cortex tracked one's own performance. Dorsomedial frontal area 9 tracked others' performances, but also integrated contextual and self-related information. Self-other mergence increased with the strength of self and other representations in area 9, suggesting it carries interdependent representations of self and other.

Value, search, persistence and model updating in anterior cingulate cortex.

Dorsal anterior cingulate cortex (dACC) carries a wealth of value-related information necessary for regulating behavioral flexibility and persistence. It signals error and reward events informing decisions about switching or staying with current behavior. During decision-making, it encodes the average value of exploring alternative choices (search value), even after controlling for response selection difficulty, and during learning, it encodes the degree to which internal models of the environment and current task must be updated. dACC value signals are derived in part from the history of recent reward integrated simultaneously over multiple time scales, thereby enabling comparison of experience over the recent and extended past. Such ACC signals may instigate attentionally demanding and difficult processes such as behavioral change via interactions with prefrontal cortex. However, the signal in dACC that instigates behavioral change need not itself be a conflict or difficulty signal.

Predictive decision making driven by multiple time-linked reward representations in the anterior cingulate cortex.

In many natural environments the value of a choice gradually gets better or worse as circumstances change. Discerning such trends makes predicting future choice values possible. We show that humans track such trends by comparing estimates of recent and past reward rates, which they are able to hold simultaneously in the dorsal anterior cingulate cortex (dACC). Comparison of recent and past reward rates with positive and negative decision weights is reflected by opposing dACC signals indexing these quantities. The relative strengths of time-linked reward representations in dACC predict whether subjects persist in their current behaviour or switch to an alternative. Computationally, trend-guided choice can be modelled by using a reinforcement-learning mechanism that computes a longer-term estimate (or expectation) of prediction errors. Using such a model, we find a relative predominance of expected prediction errors in dACC, instantaneous prediction errors in the ventral striatum and choice signals in the ventromedial prefrontal cortex.