Before and below 'theory of mind': embodied simulation and the neural correlates of social cognition

The automatic translation of folk psychology into newly formed brain modules specifically dedicated to mind-reading and other social cognitive abilities should be carefully scrutinized. Searching for the brain location of intentions, beliefs and desires-as such-might not be the best epistemic strategy to disclose what social cognition really is. The results of neurocognitive research suggest that in the brain of primates, mirror neurons, and more generally the premotor system, play a major role in several aspects of social cognition, from action and intention understanding to language processing. This evidence is presented and discussed within the theoretical frame of an embodied simulation account of social cognition. Embodied simulation and the mirror neuron system underpinning it provide the means to share communicative intentions, meaning and reference, thus granting the parity requirements of social communication.     

Association between the oxytocin receptor (OXTR) gene and children's social cognition at 18 months

At 18 months, children engage in a variety of social behaviors that reflect their nascent ability to understand the intentions of other people (e.g. joint attention, empathy, cooperation and self‐recognition). Although numerous contextual factors have been shown to predict social cognition in young children, the genetic underpinnings of social‐cognitive traits has been understudied in this age group. Owing to the known effects of oxytocin on adult social cognition and psychopathology, this study hypothesized that variability in the oxytocin receptor gene (OXTR) would be associated with social cognition in children at 18 months. Participants consisted of 350 children (182 males; 168 females) who were part of an ongoing longitudinal study that aimed to assess environmental and genetic contributions to children's cognitive and socio‐emotional functioning. At 18 months, social cognition was measured using previously validated and developmentally sensitive tasks assessing children's joint attention, empathy, cooperation and self‐recognition. Five potentially functional OXTR variants were genotyped: rs1042778, rs2254298, rs11131149, rs237897 and rs237899. A family‐based association design was used to control for population admixture and stratification, and additional non‐genomic covariates were controlled. Results showed that variability in rs11131149 was significantly associated with social cognition (P = 0.009), with more copies of the major allele related to higher social cognition, and more copies of the minor (risk) allele associated with lower social cognition. A haplotype consisting of rs11131149–rs2254298 was also associated with social cognition (P = 0.020). Implications for normative and pathological development are discussed, and key areas for future research are proposed.     

Gazing at me: the importance of social meaning in understanding direct-gaze cues

Direct gaze is an engaging and important social cue, but the meaning of direct gaze depends heavily on the surrounding context. This paper reviews some recent studies of direct gaze, to understand more about what neural and cognitive systems are engaged by this social cue and why. The data show that gaze can act as an arousal cue and can modulate actions, and can activate brain regions linked to theory of mind and self-related processing. However, all these results are strongly modulated by the social meaning of a gaze cue and by whether participants believe that another person is really watching them. The implications of these contextual effects and audience effects for our theories of gaze are considered.     

Mechanisms and development of self–other distinction in dyads and groups

This opinion piece offers a commentary on the four papers that address the theme of the development of self and other understanding with a view to highlighting the important contribution of developmental research to understanding of mechanisms of social cognition. We discuss potential mechanisms linking self–other distinction and empathy, implications for grouping motor, affective and cognitive domains under a single mechanism, applications of these accounts for joint action and finally consider self–other distinction in group versus dyadic settings.     

Social cognition and psychopathology: a critical overview

The philosophical and interdisciplinary debate about the nature of social cognition, and the processes involved, has important implications for psychiatry. On one account, mindreading depends on making theoretical inferences about another person''s mental states based on knowledge of folk psychology, the so-called “theory theory” (TT). On a different account, “simulation theory” (ST), mindreading depends on simulating the other''s mental states within one''s own mental or motor system. A third approach, “interaction theory” (IT), looks to embodied processes (involving movement, gesture, facial expression, vocal intonation, etc.) and the dynamics of intersubjective interactions (joint attention, joint action, and processes not confined to an individual system) in highly contextualized situations to explain social cognition, and disruptions of these processes in some psychopathological conditions. In this paper, we present a brief summary of these three theoretical frameworks (TT, ST, IT). We then focus on impaired social abilities in autism and schizophrenia from the perspective of the three approaches. We discuss the limitations of such approaches in the scientific studies of these and other pathologies, and we close with a short reflection on the future of the field. In this regard we argue that, to the extent that TT, ST and IT offer explanations that capture different (limited) aspects of social cognition, a pluralist approach might be best.     

Adaptations for social cognition in the primate brain

Studies of the factors affecting reproductive success in group-living monkeys have traditionally focused on competitive traits, like the acquisition of high dominance rank. Recent research, however, indicates that the ability to form cooperative social bonds has an equally strong effect on fitness. Two implications follow. First, strong social bonds make individuals'' fitness interdependent and the ‘free-rider’ problem disappears. Second, individuals must make adaptive choices that balance competition and cooperation—often with the same partners. The proximate mechanisms underlying these behaviours are only just beginning to be understood. Recent results from cognitive and systems neuroscience provide us some evidence that many social and non-social decisions are mediated ultimately by abstract, domain-general neural mechanisms. However, other populations of neurons in the orbitofrontal cortex, striatum, amygdala and parietal cortex specifically encode the type, importance and value of social information. Whether these specialized populations of neurons arise by selection or through developmental plasticity in response to the challenges of social life remains unknown. Many brain areas are homologous and show similar patterns of activity in human and non-human primates. In both groups, cortical activity is modulated by hormones like oxytocin and by the action of certain genes that may affect individual differences in behaviour. Taken together, results suggest that differences in cooperation between the two groups are a matter of degree rather than constituting a fundamental, qualitative distinction.     

Do young rhesus macaques know what others see?: A comparative developmental perspective

Humans undergo robust ontogenetic shifts in the theory of mind capabilities. Are these developmental changes unique to human development or are they shared with other closely related non-human species? To explore this issue, we tested the development of the theory of mind capacities in a population of 236 infant and juvenile rhesus macaques (Macaca mulatta). Using a looking-time method, we examined what developing monkeys know about others’ perceptions. Specifically, we tested whether younger monkeys predict that a person will reach for an object where she last saw it. Overall, we found a significant interaction between a monkey's age and performance on this task (p = .014). Juvenile monkeys (between two and 5 years of age) show a nonsignificant trend towards human infant-like patterns of performance, looking longer during the unexpected condition as compared to the expected condition, though this difference is nonsignificant (p = .09). However, contrary to findings in human infants, infant rhesus macaques show a different trend. Infant monkeys on average look slightly longer on average during the expected condition than the unexpected condition, though this pattern was not significant (p = .06). Our developmental results in monkeys provide some hints about the development of the theory of mind capacities in non-humans. First, young rhesus macaques appear to show some interest in the perception of other agents. Second, young rhesus seems able to make predictions based on the visual perspective of another agent, though the developmental pattern of this ability is not as clear nor as robust as in humans. As such, though an understanding of others’ perceptions is early-emerging in human infants, it may require more experience interacting with other social agents in our non-human relatives.     

The social brain: allowing humans to boldly go where no other species has been

The biological basis of complex human social interaction and communication has been illuminated through a coming together of various methods and disciplines. Among these are comparative studies of other species, studies of disorders of social cognition and developmental psychology. The use of neuroimaging and computational models has given weight to speculations about the evolution of social behaviour and culture in human societies. We highlight some networks of the social brain relevant to two-person interactions and consider the social signals between interacting partners that activate these networks. We make a case for distinguishing between signals that automatically trigger interaction and cooperation and ostensive signals that are used deliberately. We suggest that this ostensive signalling is needed for ‘closing the loop’ in two-person interactions, where the partners each know that they have the intention to communicate. The use of deliberate social signals can serve to increase reputation and trust and facilitates teaching. This is likely to be a critical factor in the steep cultural ascent of mankind.     

Perspective-taking abilities in the balance between autism tendencies and psychosis proneness

Difficulties with the ability to appreciate the perspective of others (mentalizing) is central to both autism and schizophrenia spectrum disorders. While the disorders are diagnostically independent, they can co-occur in the same individual. The effect of such co-morbidity is hypothesized to worsen mentalizing abilities. The recent influential ‘diametric brain theory’, however, suggests that the disorders are etiologically and phenotypically diametrical, predicting opposing effects on one''s mentalizing abilities. To test these contrasting hypotheses, we evaluated the effect of psychosis and autism tendencies on the perspective-taking (PT) abilities of 201 neurotypical adults, on the assumption that autism tendencies and psychosis proneness are heritable dimensions of normal variation. We show that while both autism tendencies and psychosis proneness induce PT errors, their interaction reduced these errors. Our study is, to our knowledge, the first to observe that co-occurring autistic and psychotic traits can exert opposing influences on performance, producing a normalizing effect possibly by way of their diametrical effects on socio-cognitive abilities. This advances the notion that some individuals may, to some extent, be buffered against developing either illness or present fewer symptoms owing to a balanced expression of autistic and psychosis liability.     

Neuroethology of reward and decision making

Ethology, the evolutionary science of behaviour, assumes that natural selection shapes behaviour and its neural substrates in humans and other animals. In this view, the nervous system of any animal comprises a suite of morphological and behavioural adaptations for solving specific information processing problems posed by the physical or social environment. Since the allocation of behaviour often reflects economic optimization of evolutionary fitness subject to physical and cognitive constraints, neurobiological studies of reward, punishment, motivation and decision making will profit from an appreciation of the information processing problems confronted by animals in their natural physical and social environments.     

Individual and social learning processes involved in the acquisition and generalization of tool use in macaques

Macaques can efficiently use several tools, but their capacity to discriminate the relevant physical features of a tool and the social factors contributing to their acquisition are still poorly explored. In a series of studies, we investigated macaques' ability to generalize the use of a stick as a tool to new objects having different physical features (study 1), or to new contexts, requiring them to adapt the previously learned motor strategy (study 2). We then assessed whether the observation of a skilled model might facilitate tool-use learning by naive observer monkeys (study 3). Results of study 1 and study 2 showed that monkeys trained to use a tool generalize this ability to tools of different shape and length, and learn to adapt their motor strategy to a new task. Study 3 demonstrated that observing a skilled model increases the observers' manipulations of a stick, thus facilitating the individual discovery of the relevant properties of this object as a tool. These findings support the view that in macaques, the motor system can be modified through tool use and that it has a limited capacity to adjust the learnt motor skills to a new context. Social factors, although important to facilitate the interaction with tools, are not crucial for tool-use learning.     

Chimpanzees predict that a competitor's preference will match their own

The ability to predict how another individual will behave is useful in social competition. Chimpanzees can predict the behaviour of another based on what they observe her to see, hear, know and infer. Here we show that chimpanzees act on the assumption that others have preferences that match their own. All subjects began with a preference for a box with a picture of food over one with a picture of nothing, even though the pictures had no causal relation to the contents. In a back-and-forth food competition, chimpanzees then avoided the box with the picture of food when their competitor had chosen one of the boxes before them—presumably on the assumption that the competitor shared their own preference for it and had already chosen it. Chimpanzees predicted that their competitor''s preference would match their own and adjusted their behavioural strategies accordingly.     

The shaping of social perception by stimulus and knowledge cues to human animacy

Although robots are becoming an ever-growing presence in society, we do not hold the same expectations for robots as we do for humans, nor do we treat them the same. As such, the ability to recognize cues to human animacy is fundamental for guiding social interactions. We review literature that demonstrates cortical networks associated with person perception, action observation and mentalizing are sensitive to human animacy information. In addition, we show that most prior research has explored stimulus properties of artificial agents (humanness of appearance or motion), with less investigation into knowledge cues (whether an agent is believed to have human or artificial origins). Therefore, currently little is known about the relationship between stimulus and knowledge cues to human animacy in terms of cognitive and brain mechanisms. Using fMRI, an elaborate belief manipulation, and human and robot avatars, we found that knowledge cues to human animacy modulate engagement of person perception and mentalizing networks, while stimulus cues to human animacy had less impact on social brain networks. These findings demonstrate that self–other similarities are not only grounded in physical features but are also shaped by prior knowledge. More broadly, as artificial agents fulfil increasingly social roles, a challenge for roboticists will be to manage the impact of pre-conceived beliefs while optimizing human-like design.     

Nonsocial and social cognition in schizophrenia: current evidence and future directions

Cognitive impairment in schizophrenia involves a broad array of nonsocial and social cognitive domains. It is a core feature of the illness, and one with substantial implications for treatment and prognosis. Our understanding of the causes, consequences and interventions for cognitive impairment in schizophrenia has grown substantially in recent years. Here we review a range of topics, including: a) the types of nonsocial cognitive, social cognitive, and perceptual deficits in schizophrenia; b) how deficits in schizophrenia are similar or different from those in other disorders; c) cognitive impairments in the prodromal period and over the lifespan in schizophrenia; d) neuroimaging of the neural substrates of nonsocial and social cognition, and e) relationships of nonsocial and social cognition to functional outcome. The paper also reviews the considerable efforts that have been directed to improve cognitive impairments in schizophrenia through novel psychopharmacology, cognitive remediation, social cognitive training, and alternative approaches. In the final section, we consider areas that are emerging and have the potential to provide future insights, including the interface of motivation and cognition, the influence of childhood adversity, metacognition, the role of neuroinflammation, computational modelling, the application of remote digital technology, and novel methods to evaluate brain network organization. The study of cognitive impairment has provided a way to approach, examine and comprehend a wide range of features of schizophrenia, and it may ultimately affect how we define and diagnose this complex disorder.     

Early false-belief understanding in traditional non-Western societies

The psychological capacity to recognize that others may hold and act on false beliefs has been proposed to reflect an evolved, species-typical adaptation for social reasoning in humans; however, controversy surrounds the developmental timing and universality of this trait. Cross-cultural studies using elicited-response tasks indicate that the age at which children begin to understand false beliefs ranges from 4 to 7 years across societies, whereas studies using spontaneous-response tasks with Western children indicate that false-belief understanding emerges much earlier, consistent with the hypothesis that false-belief understanding is a psychological adaptation that is universally present in early childhood. To evaluate this hypothesis, we used three spontaneous-response tasks that have revealed early false-belief understanding in the West to test young children in three traditional, non-Western societies: Salar (China), Shuar/Colono (Ecuador) and Yasawan (Fiji). Results were comparable with those from the West, supporting the hypothesis that false-belief understanding reflects an adaptation that is universally present early in development.     

Neural signatures for sustaining object representations attributed to others in preverbal human infants

A major feat of social beings is to encode what their conspecifics see, know or believe. While various non-human animals show precursors of these abilities, humans perform uniquely sophisticated inferences about other people''s mental states. However, it is still unclear how these possibly human-specific capacities develop and whether preverbal infants, similarly to adults, form representations of other agents'' mental states, specifically metarepresentations. We explored the neurocognitive bases of eight-month-olds'' ability to encode the world from another person''s perspective, using gamma-band electroencephalographic activity over the temporal lobes, an established neural signature for sustained object representation after occlusion. We observed such gamma-band activity when an object was occluded from the infants'' perspective, as well as when it was occluded only from the other person (study 1), and also when subsequently the object disappeared, but the person falsely believed the object to be present (study 2). These findings suggest that the cognitive systems involved in representing the world from infants'' own perspective are also recruited for encoding others'' beliefs. Such results point to an early-developing, powerful apparatus suitable to deal with multiple concurrent representations, and suggest that infants can have a metarepresentational understanding of other minds even before the onset of language.