Oxytocin,testosterone, and human social cognition

I describe an integrative social‐evolutionary model for the adaptive significance of the human oxytocinergic system. The model is based on a role for this hormone in the generation and maintenance of social familiarity and affiliation across five homologous, functionally similar, and sequentially co‐opted contexts: mothers with offspring, female and male mates, kin groups, individuals with reciprocity partners, and individuals within cooperating and competing social groups defined by culture. In each situation, oxytocin motivates, mediates and rewards the cognitive and behavioural processes that underlie the formation and dynamics of a more or less stable social group, and promotes a relationship between two or more individuals. Such relationships may be positive (eliciting neurological reward, reducing anxiety and thus indicating fitness‐enhancing effects), or negative (increasing anxiety and distress, and thus motivating attempts to alleviate a problematic, fitness‐reducing social situation). I also present evidence that testosterone exhibits opposite effects from oxytocin on diverse aspects of cognition and behaviour, most generally by favouring self‐oriented, asocial and antisocial behaviours. I apply this model for effects of oxytocin and testosterone to understanding human psychological disorders centrally involving social behaviour. Reduced oxytocin and higher testosterone levels have been associated with under‐developed social cognition, especially in autism. By contrast, some combination of oxytocin increased above normal levels, and lower testosterone, has been reported in a notable number of studies of schizophrenia, bipolar disorder and depression, and, in some cases, higher oxytocin involves maladaptively ‘hyper‐developed’ social cognition in these conditions. This pattern of findings suggests that human social cognition and behaviour are structured, in part, by joint and opposing effects of oxytocin and testosterone, and that extremes of such joint effects partially mediate risks and phenotypes of autism and psychotic‐affective conditions. These considerations have direct implications for the development of therapies for alleviating disorders of social cognition, and for understanding how such disorders are associated with the evolution of human cognitive‐affective architecture.     

Animal morality: What is the debate about?

Empirical studies of the social lives of non-human primates, cetaceans, and other social animals have prompted scientists and philosophers to debate the question of whether morality and moral cognition exists in non-human animals. Some researchers have argued that morality does exist in several animal species, others that these species may possess various evolutionary building blocks or precursors to morality, but not quite the genuine article, while some have argued that nothing remotely resembling morality can be found in any non-human species. However, these different positions on animal morality generally appear to be motivated more by different conceptions of how the term “morality” is to be defined than by empirical disagreements about animal social behaviour and psychology. After delving deeper into the goals and methodologies of various of the protagonists, I argue that, despite appearances, there are actually two importantly distinct debates over animal morality going on, corresponding to two quite different ways of thinking about what it is to define “morality”, “moral cognition”, and associated notions. Several apparent skirmishes in the literature are thus cases of researchers simply talking past each other. I then focus on what I take to be the core debate over animal morality, which is concerned with understanding the nature and phylogenetic distribution of morality conceived as a psychological natural kind. I argue that this debate is in fact largely terminological and non-substantive. Finally, I reflect on how this core debate might best be re-framed.     

The social nature of primate cognition

The hypothesis that the enlarged brain size of the primates was selected for by social, rather than purely ecological, factors has been strongly influential in studies of primate cognition and behaviour over the past two decades. However, the Machiavellian intelligence hypothesis, also known as the social brain hypothesis, tends to emphasize certain traits and behaviours, like exploitation and deception, at the expense of others, such as tolerance and behavioural coordination, and therefore presents only one view of how social life may shape cognition. This review outlines work from other relevant disciplines, including evolutionary economics, cognitive science and neurophysiology, to illustrate how these can be used to build a more general theoretical framework, incorporating notions of embodied and distributed cognition, in which to situate questions concerning the evolution of primate social cognition.     

Ruthless reductionism and social cognition

Social cognition appears to present phenomena that "ruthlessly reductive" molecular and cellular neuroscience cannot fruitfully investigate or explain. This is because the causes of such phenomena are distal and external not only to the molecular machinery of individual neurons, but to individual brains. However, the "reductionist's epiphany" insists that to the extent that we understand the specific molecular mechanisms that underlie phenomena upon which most or all social cognition depends, we can be sure that molecular mechanisms for the broader phenomena can be found using standard experimental methods from molecular and cellular cognition. Furthermore, social recognition memory consolidation is required for virtually all types of social cognition, and its specific molecular mechanisms have now been uncovered experimentally. These same molecular mechanisms obtain across a wide variety of divergent species (from invertebrates to vertebrates). Thus we can expect to find the molecular mechanisms of the broader social cognitive functions that must "plug into" these specific molecular mechanisms, despite these functions' typically distal, external initial causes. This conclusion rests on explicit scientific facts, not just on some vague philosophical commitment to physicalism about mind.     

Comparative social cognition: what can dogs teach us?

Research in comparative social cognition addresses how challenges of social living have formed the cognitive structures that control behaviours involved in communication, social learning and social understanding. In contrast to the traditional psychological approach, recent investigations take both evolutionary and functional questions into account, but the main emphasis is still on the mechanisms of behaviour. Although in traditional research ‘comparative’ meant mainly comparisons between humans and other primates, ethological influences have led to a broadening of the spectrum of species under study. In this review, we evaluated how the study of dogs broadens our understanding of comparative social cognition. In the early days of ethology, dogs enjoyed considerable interest from ethologists, but during the last 20 years, dogs have rarely been studied by ethological methods. Through a complex evolutionary process, dogs became adapted for living in human society; therefore, the human environment and social setting now represents a natural ecological niche for this species. We have evidence that dogs have been selected for adaptations to human social life, and that these adaptations have led to marked changes in their communicative, social, cooperative and attachment behaviours towards humans. Until now, the study of dogs was hindered by the view that they represent an ‘artificial’ species, but by accepting that dogs are adapted to their niche, as are other ‘natural’ species, comparative investigations can be put into new light.     

Brain imaging investigation of the neural correlates of observing virtual social interactions

The ability to gauge social interactions is crucial in the assessment of others' intentions. Factors such as facial expressions and body language affect our decisions in personal and professional life alike (1). These "friend or foe" judgements are often based on first impressions, which in turn may affect our decisions to "approach or avoid". Previous studies investigating the neural correlates of social cognition tended to use static facial stimuli (2). Here, we illustrate an experimental design in which whole-body animated characters were used in conjunction with functional magnetic resonance imaging (fMRI) recordings. Fifteen participants were presented with short movie-clips of guest-host interactions in a business setting, while fMRI data were recorded; at the end of each movie, participants also provided ratings of the host behaviour. This design mimics more closely real-life situations, and hence may contribute to better understanding of the neural mechanisms of social interactions in healthy behaviour, and to gaining insight into possible causes of deficits in social behaviour in such clinical conditions as social anxiety and autism (3).     

Do Online Voting Patterns Reflect Evolved Features of Human Cognition? An Exploratory Empirical Investigation

Online votes or ratings can assist internet users in evaluating the credibility and appeal of the information which they encounter. For example, aggregator websites such as Reddit allow users to up-vote submitted content to make it more prominent, and down-vote content to make it less prominent. Here we argue that decisions over what to up- or down-vote may be guided by evolved features of human cognition. We predict that internet users should be more likely to up-vote content that others have also up-voted (social influence), content that has been submitted by particularly liked or respected users (model-based bias), content that constitutes evolutionarily salient or relevant information (content bias), and content that follows group norms and, in particular, prosocial norms. 489 respondents from the online social voting community Reddit rated the extent to which they felt different traits influenced their voting. Statistical analyses confirmed that norm-following and prosociality, as well as various content biases such as emotional content and originality, were rated as important motivators of voting. Social influence had a smaller effect than expected, while attitudes towards the submitter had little effect. This exploratory empirical investigation suggests that online voting communities can provide an important test-bed for evolutionary theories of human social information use, and that evolved features of human cognition may guide online behaviour just as it guides behaviour in the offline world.     

A guide to practical babooning: Historical,social, and cognitive contingency

As ecologically adaptable animals, baboons are distributed widely across Africa, and display a variety of morphological and behavioral differences that reflect both local ecology and a complex evolutionary history. As long‐lived, slowly reproducing animals, baboons face numerous ecological challenges to survival and successful reproduction. As group‐living animals, the social world presents an equally diverse array of challenges that require the negotiation of individual needs within the constraints imposed by others. Understanding how all these facets of baboon evolutionary history, life history, ecology, sociality, and cognition fit together is an enormous but engaging challenge, and despite one hundred years of study, it is clear there is a still much to learn about the various natural histories of baboons. What also is clear, however, is that an appreciation of contingency holds the key to understanding all these facets of baboon evolution and behavior. In what follows, I hope to illustrate exactly what I mean by this, highlighting along the way that history is not to be ignored, variability is information and not merely “noise”, and that behavioral and cognitive complexity can be two very different things.     

Hominid cultural transmission and the evolution of language

This paper presents the hypothesis that linguistic capacity evolved through the action of natural selection as an instrument which increased the efficiency of the cultural transmission system of early hominids. We suggest that during the early stages of hominization, hominid social learning, based on indirect social learning mechanisms and true imitation, came to constitute cumulative cultural transmission based on true imitation and the approval or disapproval of the learned behaviour of offspring. A key factor for this transformation was the development of a conceptual capacity for categorizing learned behaviour in value terms - positive or negative, good or bad. We believe that some hominids developed this capacity for categorizing behaviour, and such an ability allowed them to approve or disapprove of their offsprings- learned behaviour. With such an ability, hominids were favoured, as they could transmit to their offspring all their behavioural experience about what can and cannot be done. This capacity triggered a cultural transmission system similar to the human one, though pre-linguistic. We suggest that the adaptive advantage provided by this new system of social learning generated a selection pressure in favour of the development of a linguistic capacity allowing children to better understand the new kind of evaluative information received from parents.     

Evidence for social role in a dolphin social network

Social animals have to take into consideration the behaviour of conspecifics when making decisions to go by their daily lives. These decisions affect their fitness and there is therefore an evolutionary pressure to try making the right choices. In many instances individuals will make their own choices and the behaviour of the group will be a democratic integration of everyone’s decision. However, in some instances it can be advantageous to follow the choice of a few individuals in the group if they have more information regarding the situation that has arisen. Here I provide early evidence that decisions about shifts in activity states in a population of bottlenose dolphin follow such a decision-making process. This unshared consensus is mediated by a non-vocal signal, which can be communicated globally within the dolphin school. These signals are emitted by individuals that tend to have more information about the behaviour of potential competitors because of their position in the social network. I hypothesise that this decision-making process emerged from the social structure of the population and the need to maintain mixed-sex schools.     

Conflicting social norms and community conservation compliance

Though the success of conservation initiatives relies on changing behaviour, little social psychological research has examined factors such as attitudes and social norms in the context of actual conservation campaigns. In the context of reducing light pollution around sea turtle nesting habitats, researching technological solutions has clear merit. Problems such as light glow are, however, fundamentally about human behaviour, and so finding ways to effect behavioural change is critical. Social norms, or perceptions about what other people think and do, have been widely used in behaviour change campaigns across various domains, including campaigns to promote conservation behaviour. Here, we investigate how the norms of different groups may influence our behaviour in the context of a campaign to alter behavioural norms about light glow pollution in a community. We examine attitudes, social norms, and the degree of conflict (versus congruence) between the behaviours of different groups, and their relationship with intentions to engage in conservation behaviours relevant to sea turtle conservation. We show that attitudes and norms are related to behavioural intentions, and conflicts between social norms influence intentions, over and above the norms themselves. This highlights an important consideration for conservation campaigns utilising social norms-based behaviour change appeals.     

Selfish altruism,fierce cooperation and the predator*

This paper suggests a new way to think about a famous question: what explains cooperation in nature and in particular in humans? I argue that, for an evolutionary biologist as well as a quantitative social scientist, the triangle of two ‘teammates’ in the presence of a predator (passing and shooting in two-on-one situations) is one of the fundamental conceptual building-blocks for understanding these phenomena because in such a situation the fact that life is packaged in many distinct enclosures (and not in one big monolithic blob) can unfold its comparative advantage. I show how, in the presence of a predator, cooperative equilibria emerge among entirely selfish teammates if we infinitesimally bias the lead player in the selfish direction or assign a computational burden on the predator due to the presence of a teammate. I argue that ‘predators’ are common in the biological jungle but also in everyday human settings. Intuitively, this paper builds on the simple idea – a familiar one to a biologist observing the natural world but perhaps less so to social scientists – that everybody has enemies.     

Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine

The neuropeptides oxytocin (OXT) and arginine vasopressin (AVP) are evolutionarily highly conserved mediators in the regulation of complex social cognition and behaviour. Recent studies have investigated the effects of OXT and AVP on human social interaction, the genetic mechanisms of inter-individual variation in social neuropeptide signalling and the actions of OXT and AVP in the human brain as revealed by neuroimaging. These data have advanced our understanding of the mechanisms by which these neuropeptides contribute to human social behaviour. OXT and AVP are emerging as targets for novel treatment approaches--particularly in synergistic combination with psychotherapy--for mental disorders characterized by social dysfunction, such as autism, social anxiety disorder, borderline personality disorder and schizophrenia.     

Adaptivity of social systems: the problem for scientific research

The notion of adaptive evolution of social systems as of a real process of selection of the properties of such systems implies group selection. But strong evidences of effective group selection seem impossible, at least in vertebrates. However, understanding the origin of social systems adaptivity based on individual selection is difficult, as well, without analyzing the proximal mechanisms of the formation of such systems. I suppose that social systems change due to changes of individual features that underlie the proximal mechanisms of the system formation. These features are the characteristics of neurophysiological and hormonal regulatory mechanisms. They are strongly associated with intrinsic biochemical processes and are coded in the genome. Thus, the evolution of social systems is the evolution of their proximal mechanisms. At the same time, the specificity of neurophysiological and hormonal regulation determines not only social interactions, but also the individual behaviour of animals. The most important characteristics of life history, such as the regime of activity, foraging strategy, etc., are strongly affected by the same regulatory mechanisms. This view is useful for understanding the relations combining many features into an integrated and adaptive species-specific life form. I suppose that such forms emerged as evolutionary consequences of changes in regulatory mechanisms adaptive to specific environment. Thus, we have as substantial reasons to discuss adaptations of social systems to ecological features as to discuss ecological features adapted to particular social systems. The species-specificity of regulatory mechanisms is probably based on different kinds of evolutionary choice between the rapidity and the perfection of adaptation, between flexibility and stability, and between sensibility and resistibility. I think that this choice depends largely on the predictability of the environment. The less predictable it is, the more it increases the selective value of sensibility, flexibility, and rapidity of evolution. On the contrary, stable and predictable environment stimulates less rapid but more perfect adaptations. Such choices consolidate in the genome during evolution as specific features of neurophysiological and hormonal regulation systems. These specific features, in their turn, determine ecological, behavioural, and physiological species-specificity. From this point of view, evolutionary changes in social systems can be readily perceived as consequences of the selection of individuals, promoting optimal properties under particular conditional features of regulation systems. The boundary condition for this model is the absence of specificity of the characteristics of regulation systems to different forms of stress. This condition needs to be considered closely.     

The origins of belonging: social motivation in infants and young children

Our reliance on our group members has exerted a profound influence over our motivation: successful group functioning requires that we are motivated to interact, and engage, with those around us. In other words, we need to belong. In this article, I explore the developmental origins of our need to belong. I discuss existing evidence that, from early in development, children seek to affiliate with others and to form long-lasting bonds with their group members. Furthermore, when children are deprived of a sense of belonging, it has negative consequences for their well-being. This focus on social motivation enables us to examine why and in what circumstances children engage in particular behaviours. It thus provides an important complement to research on social cognition. In doing so, it opens up important questions for future research and provides a much-needed bridge between developmental and social psychology.     

Network-based diffusion analysis: a new method for detecting social learning

Social learning has been documented in a wide diversity of animals. In free-living animals, however, it has been difficult to discern whether animals learn socially by observing other group members or asocially by acquiring a new behaviour independently. We addressed this challenge by developing network-based diffusion analysis (NBDA), which analyses the spread of traits through animal groups and takes into account that social network structure directs social learning opportunities. NBDA fits agent-based models of social and asocial learning to the observed data using maximum-likelihood estimation. The underlying learning mechanism can then be identified using model selection based on the Akaike information criterion. We tested our method with artificially created learning data that are based on a real-world co-feeding network of macaques. NBDA is better able to discriminate between social and asocial learning in comparison with diffusion curve analysis, the main method that was previously applied in this context. NBDA thus offers a new, more reliable statistical test of learning mechanisms. In addition, it can be used to address a wide range of questions related to social learning, such as identifying behavioural strategies used by animals when deciding whom to copy.     

Interindividual variability in social insects – proximate causes and ultimate consequences

Individuals within social groups often show consistent differences in behaviour across time and context. Such interindividual differences and the evolutionary challenge they present have recently generated considerable interest. Social insects provide some of the most familiar and spectacular examples of social groups with large interindividual differences. Investigating these within‐group differences has a long research tradition, and behavioural variability among the workers of a colony is increasingly regarded as fundamental for a key feature of social insects: division of labour. The goal of this review is to illustrate what we know about both the proximate mechanisms underlying behavioural variability among the workers of a colony and its ultimate consequences; and to highlight the many open questions in this research field. We begin by reviewing the literature on mechanisms that potentially introduce, maintain, and adjust the behavioural differentiation among workers. We highlight the fact that so far, most studies have focused on behavioural variability based on genetic variability, provided by e.g. multiple mating of the queen, while other mechanisms that may be responsible for the behavioural differentiation among workers have been largely neglected. These include maturational, nutritional and environmental influences. We further discuss how feedback provided by the social environment and learning and experience of adult workers provides potent and little‐explored sources of differentiation. In a second part, we address what is known about the potential benefits and costs of increased behavioural variability within the workers of a colony. We argue that all studies documenting a benefit of variability so far have done so by manipulating genetic variability, and that a direct test of the effect of behavioural variability on colony productivity has yet to be provided. We emphasize that the costs associated with interindividual variability have been largely overlooked, and that a better knowledge of the cost/benefit balance of behavioural variability is crucial for our understanding of the evolution of the mechanisms underlying the social organization of insect societies. We conclude by highlighting what we believe to be promising but little‐explored avenues for future research on how within‐colony variability has evolved and is maintained. We emphasize the need for comparative studies and point out that, so far, most studies on interindividual variability have focused on variability in individual response thresholds, while the significance of variability in other parameters of individual response, such as probability and intensity of the response, has been largely overlooked. We propose that these parameters have important consequences for the colony response. Much more research is needed to understand if and how interindividual variability is modulated in order to benefit division of labour, homeostasis and ultimately colony fitness in social insects.     

Social structure and indirect genetic effects: genetics of social behaviour

The social environment modulates gene expression, physiology, behaviour and patterns of inheritance. For more than 50 years, this concept has been investigated using approaches that include partitioning the social component out of behavioural heritability estimates, studying maternal effects on offspring, and analysing dominance hierarchies. Recent advances have formalized this ‘social environment effect’ by providing a more nuanced approach to the study of social influences on behaviour while recognizing evolutionary implications. Yet, in most of these formulations, the dynamics of social interactions are not accounted for. Also, the reciprocity between individual behaviour and group‐level interactions has been largely ignored. Consistent with evolutionary theory, the principles of social interaction are conserved across a broad range of taxa. While noting parallels in diverse organisms, this review uses Drosophila melanogaster as a case study to revisit what is known about social interaction paradigms. We highlight the benefits of integrating the history and pattern of interactions among individuals for dissecting molecular mechanisms that underlie social modulation of behaviour.     

Social neuroscience of disgust

Disgust can be thought of as an affective system that has evolved to detect signs of pathogens, parasite and toxins as well as to stimulate behaviors that reduce the risk of their acquisition. Disgust incorporates social cognitive mechanisms to regulate exposure to and, or anticipate and avoid exposure to pathogens and toxins. Social cognition entails the acquisition of social information about others (ie, social recognition) and from others (ie, social learning). This involves recognizing and assessing other individuals and the pathogen/parasite/contamination/toxin threat they pose and deciding about when and how to interact with and, or avoid them. Social cognition provides a frame‐work for examining the expression of disgust and the associated neurobiological mechanisms. Here, we briefly consider the relations between social cognition and pathogen/parasite/toxin avoidance behaviors. We briefly discuss aspects of: (1) the odor mediated social recognition of actual and potentially infected individuals and the impact of parasite/pathogen threat on disgust mate and social partner choice; (2) the roles of “out‐groups” (strangers, unfamiliar individuals) and “in‐groups” (familiar individuals) in the expression of disgust and pathogen avoidance behaviors; (3) individual and social learning of disgust and empathy for disgust; (4) toxin elicited disgust and anticipatory disgust; (5) the neurobiological mechanisms, and in particular the roles of the nonapeptide, oxytocin and estrogenic mechanism associated with social cognition and the expression of disgust. These findings on the social neuroscience of disgust have a direct bearing on our understanding of the roles of disgust in shaping human and nonhuman social behavior.