On the murky dissociation between expression and communication.

The authors present an ambitious attempt to outline the gradual evolution of the cognitive foundations of ostensive communication. We focus on three problematic aspects of the distinction between expression and communication: ambiguity in the distinction's central principle of "complementary mechanisms," inconsistencies in the application of the distinction across taxa, and the dismissal of mentalizing in nonhuman primates.

Primates unleashed.

Before claiming major differences between the communication systems of humans and other species, it is necessary to (1) overcome methodological limitations in the comparative study of communicative intentions; (2) account for mechanisms other than epistemic vigilance that may also sustain complex forms of communication; and (3) better differentiate between motivational and cognitive factors potentially affecting the emergence of open-ended communication.

Variation in communicative complexity in relation to social structure and organization in non-human primates.

Communicative complexity relates to social complexity, as individuals in more complex social systems either use more signals or more complex signals than individuals living in less complex ones. Taking the individual group member's perspective, here we examine communicative complexity in relation to social complexity, which arises from two components of social systems: social structure and social organization. We review the concepts of social relationships and social complexity and evaluate their implications for communicative and cognitive complexity using examples from primate species. We focus on spider monkeys (Ateles geoffroyi), as their social organization is characterized by flexibility in grouping dynamics and they use a variety of communicative signals. We conclude that no simple relationship exists among social complexity, communicative complexity and cognitive complexity, with social complexity not necessarily implying cognitive complexity, and communicative and cognitive complexity being independently linked to social complexity. To better understand the commonly implied link between social complexity and cognitive complexity it is crucial to recognize the complementary role of communicative complexity. A more elaborated communicative toolkit provides the needed flexibility to deal with dynamic and multifaceted social relationships and high variation in fission-fusion dynamics. This article is part of the theme issue 'Cognition, communication and social bonds in primates'.

Communicative roots of complex sociality and cognition: neuropsychological mechanisms underpinning the processing of social information.

Primate social bonds are described as being especially complex in their nature, and primates have unusually large brains for their body size compared to other mammals. Communication in primates has attracted considerable attention because of the important role it plays in social bonding. It has been proposed that differentiated social relationships are cognitively complex because primates need to continuously update their knowledge about different types of social bonds. Therefore, primates infer whether an opportunity for social interaction is rewarding (valuable to individual goals) based on their knowledge of the social relationships of the interactants. However, exposure to distraction and stress has detrimental effects on the dopaminergic system, suggesting that understanding social relationships as rewarding is affected in these conditions. This paper proposes that complex communication evolved to augment the capacity to form social relationships during stress through flexibly modifying intentionality in communication (audience checking, response waiting and elaboration). Intentional communication may upregulate dopamine dynamics to allow recognition that an interaction is rewarding during stress. By examining these associations between complexity of communication and stress, we provide new insights into the cognitive skills involved in forming social bonds in primates and the evolution of communication systems in both primates and humans. This article is part of the theme issue 'Cognition, communication and social bonds in primates'.

Socioecological complexity in primate groups and its cognitive correlates.

Characterizing non-human primate social complexity and its cognitive bases has proved challenging. Using principal component analyses, we show that primate social, ecological and reproductive behaviours condense into two components: socioecological complexity (including most social and ecological variables) and reproductive cooperation (comprising mainly a suite of behaviours associated with pairbonded monogamy). We contextualize these results using a meta-analysis of 44 published analyses of primate brain evolution. These studies yield two main consistent results: cognition, sociality and cooperative behaviours are associated with absolute brain volume, neocortex size and neocortex ratio, whereas diet composition and life history are consistently associated with relative brain size. We use a path analysis to evaluate the causal relationships among these variables, demonstrating that social group size is predicted by the neocortex, whereas ecological traits are predicted by the volume of brain structures other than the neocortex. That a range of social and technical behaviours covary, and are correlated with social group size and brain size, suggests that primate cognition has evolved along a continuum resulting in an increasingly flexible, domain-general capacity to solve a range of socioecological challenges culminating in a capacity for, and reliance on, innovation and social information use in the great apes and humans. This article is part of the theme issue 'Cognition, communication and social bonds in primates'.

Do zoo-housed primates retreat from crowds? A simple study of five primate species.

An animal's welfare state is directly influenced by the mental state, which is shaped by experiences within the environment throughout the animal's life. For zoo-housed animals, visitors to the zoo are a large part of that environment and a fluctuating influence within it. This study examines the impact of zoo visitors on the space use of five species of zoo-housed primates (Eastern black-and-white colobus monkeys, Colobus guereza, n = 5, Allen's swamp monkeys, Allenopithecus nigroviridis, n = 2, DeBrazza's monkeys, Cercopithecus neglectus, n = 3, Bolivian gray titi monkeys, Callicebus donacophilus, n = 3, and crowned lemurs, Eulemur coronatus, n = 3). Specifically, we considered whether primates' distance from visitor areas changed as crowd sizes increased. Data were collected using the ZooMonitor app. Observers recorded spatial coordinates for each animal over periods ranging from 12 to 32 months. Data were analyzed using two types of regression models (linear and logistic) to examine the influence of visitors on the location of the primates. Both analyses revealed a statistically significant but small decrease in primate distance from visitor viewing glass as the number of visitors increased. Behavioral indicators of welfare were also unaffected by the presence of visitors. These results suggest that, with additional validation, distance from visitors may be one promising, simple way to evaluate the influence of visitors on primate welfare.

Nonhuman primate abnormal behavior: Etiology, assessment, and treatment.

Across captive settings, nonhuman primates may develop an array of abnormal behaviors including stereotypic and self-injurious behavior. Abnormal behavior can indicate a state of poor welfare, since it is often associated with a suboptimal environment. However, this may not always be the case as some behaviors can develop independently of any psychological distress, be triggered in environments known to promote welfare, and be part of an animal's coping mechanism. Furthermore, not all animals develop abnormal behavior, which has led researchers to assess risk factors that differentiate individuals in the display of these behaviors. Intrinsic risk factors that have been identified include the animal's species and genetics, age, sex, temperament, and clinical condition, while environmental risk factors include variables such as the animal's rearing, housing condition, husbandry procedures, and research experiences. To identify specific triggers and at-risk animals, the expression of abnormal behavior in captive nonhuman primates should be routinely addressed in a consistent manner by appropriately trained staff. Which behaviors to assess, what assessment methods to use, which primates to monitor, and the aims of data collection should all be identified before proceeding to an intervention and/or treatment. This article provides guidance for this process, by presenting an overview of known triggers and risk factors that should be considered, steps to design a comprehensive evaluation plan, and strategies that might be used for prevention or treatment. It also outlines the tools and processes for assessing and evaluating behavior in an appendix. This process will lead to a better understanding of abnormal behavior in captive primate colonies and ultimately to improved welfare.

Experts in action: why we need an embodied social brain hypothesis.

The anthropoid primates are known for their intense sociality and large brain size. The idea that these might be causally related has given rise to a large body of work testing the 'social brain hypothesis'. Here, the emphasis has been placed on the political demands of social life, and the cognitive skills that would enable animals to track the machinations of other minds in metarepresentational ways. It seems to us that this position risks losing touch with the fact that brains primarily evolved to enable the control of action, which in turn leads us to downplay or neglect the importance of the physical body in a material world full of bodies and other objects. As an alternative, we offer a view of primate brain and social evolution that is grounded in the body and action, rather than minds and metarepresentation. This article is part of the theme issue 'Systems neuroscience through the lens of evolutionary theory'.

Social agent identity cells in the prefrontal cortex of interacting groups of primates.

The ability to interact effectively within social groups is essential to primate and human behavior. Yet understanding the neural processes that underlie the interactive behavior of groups or by which neurons solve the basic problem of coding for multiple agents has remained a challenge. By tracking the interindividual dynamics of groups of three interacting rhesus macaques, we discover detailed representations of the groups' behavior by neurons in the dorsomedial prefrontal cortex, reflecting not only the other agents' identities but also their specific interactions, social context, actions, and outcomes. We show how these cells collectively represent the interaction between specific group members and their reciprocation, retaliation, and past behaviors. We also show how they influence the animals' own upcoming decisions and their ability to form beneficial agent-specific interactions. Together, these findings reveal prefrontal neurons that code for the agency identity of others and a cellular mechanism that could support the interactive behavior of social groups.

Multilevel rhythms in multimodal communication.

It is now widely accepted that the brunt of animal communication is conducted via several modalities, e.g. acoustic and visual, either simultaneously or sequentially. This is a laudable multimodal turn relative to traditional accounts of temporal aspects of animal communication which have focused on a single modality at a time. However, the fields that are currently contributing to the study of multimodal communication are highly varied, and still largely disconnected given their sole focus on a particular level of description or their particular concern with human or non-human animals. Here, we provide an integrative overview of converging findings that show how multimodal processes occurring at neural, bodily, as well as social interactional levels each contribute uniquely to the complex rhythms that characterize communication in human and non-human animals. Though we address findings for each of these levels independently, we conclude that the most important challenge in this field is to identify how processes at these different levels connect. This article is part of the theme issue 'Synchrony and rhythm interaction: from the brain to behavioural ecology'.

Rhythm in dyadic interactions.

This review paper discusses rhythmic interactions and distinguishes them from non-rhythmic interactions. We report on communicative behaviours in social and sexual contexts, as found in dyads of humans, non-human primates, non-primate mammals, birds, anurans and insects. We discuss observed instances of rhythm in dyadic interactions, identify knowledge gaps and propose suggestions for future research. We find that most studies on rhythmicity in interactive signals mainly focus on one modality (acoustic or visual) and we suggest more work should be performed on multimodal signals. Although the social functions of interactive rhythms have been fairly well described, developmental research on rhythms used to regulate social interactions is still lacking. Future work should also focus on identifying the exact timing mechanisms involved. Rhythmic signalling behaviours are widespread and critical in regulating social interactions across taxa, but many questions remain unexplored. A multidisciplinary, comparative cross-species approach may help provide answers. This article is part of the theme issue 'Synchrony and rhythm interaction: from the brain to behavioural ecology'.

What emotions might be like in other animals.

In this My word, Joseph LeDoux explores what the emotional lives of other mammals might be like. He proposes that better understanding of the brain mechanisms of emotional consciousness in humans might shed light on the kinds of conscious capacities that might be possible in non-human primates and non-primate mammals, given the kinds of brains they possess.

Assessing the reliability of an automated method for measuring dominance hierarchy in non-human primates.

Among animal societies, dominance is an important social factor that influences inter-individual relationships. However, assessing dominance hierarchy can be a time-consuming activity which is potentially impeded by environmental factors, difficulties in the recognition of animals, or disturbance of animals during data collection. Here we took advantage of novel devices, machines for automated learning and testing (MALT), designed primarily to study non-human primate cognition, to additionally measure the dominance hierarchy of a semi-free-ranging primate group. When working on a MALT, an animal can be replaced by another, which could reflect an asymmetric dominance relationship. To assess the reliability of our method, we analysed a sample of the automated conflicts with video scoring and found that 74% of these replacements included genuine forms of social displacements. In 10% of the cases, we did not identify social interactions and in the remaining 16% we observed affiliative contacts between the monkeys. We analysed months of daily use of MALT by up to 26 semi-free-ranging Tonkean macaques (Macaca tonkeana) and found that dominance relationships inferred from these interactions strongly correlated with the ones derived from observations of spontaneous agonistic interactions collected during the same time period. An optional filtering procedure designed to exclude chance-driven displacements or affiliative contacts suggests that the presence of 26% of these interactions in data sets did not impair the reliability of this new method. We demonstrate that this method can be used to assess the dynamics of both individual social status, and group-wide hierarchical stability longitudinally with minimal research labour. Further, it facilitates a continuous assessment of dominance hierarchies in captive groups, even during unpredictable environmental or challenging social events, which underlines the usefulness of this method for group management purposes. Altogether, this study supports the use of MALT as a reliable tool to automatically and dynamically assess dominance hierarchy within captive groups of non-human primates, including juveniles, under conditions in which such technology can be used.

Conditional valuation for combinations of goods in primates.

Valuing goods and selecting the one with the highest value forms the basis of adaptive behaviour across species. While it is obvious that the valuation of a given type of goods depends on ownership and availability of that type of goods, the effects of other goods on valuation of the original good are sometimes underappreciated. Yet, goods interact with each other, indicating that the valuation of a given good is conditional on the other goods it is combined with, both in the wild and the laboratory. Here, we introduce conditional valuation in the context of valuing multiple goods and briefly review how human and animal experimentalists can leverage economic tools for the study of interactions among goods. We then review evidence for conditional valuation for combined foods in both human and non-human primates. In the laboratory, non-human primates show increased valuation of certain combinations of foods but decreased valuation of other types of combinations. Thus, similarly to humans, monkeys appear to value combinations of goods in a conditional fashion. Additionally, both humans and monkeys appear to employ similar neural substrates for the valuation of single goods, such as the orbitofrontal cortex. Together, investigations of our evolutionary precursors may provide insights on how we value interacting goods. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

Economic behaviours among non-human primates.

Do we have any valid reasons to affirm that non-human primates display economic behaviour in a sufficiently rich and precise sense of the phrase? To address this question, we have to develop a set of criteria to assess the vast array of experimental studies and field observations on individual cognitive and behavioural competences as well as the collective organization of non-human primates. We review a sample of these studies and assess how they answer to the following four main challenges. (i) Do we see any economic organization or institutions emerge among groups of non-human primates? (ii) Are the cognitive abilities, and often biases, that have been evidenced as underlying typical economic decision-making among humans, also present among non-human primates? (iii) Can we draw positive lessons from performance comparisons among primate species, humans and non-humans but also across non-human primate species, as elicited by canonical game-theoretical experimental paradigms, especially as far as economic cooperation and coordination are concerned? And (iv) in which way should we improve models and paradigms to obtain more ecological data and conclusions? Articles discussed in this paper most often bring about positive answers and promising perspectives to support the existence and prevalence of economic behaviours among non-human primates. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

The description-experience gap: a challenge for the neuroeconomics of decision-making under uncertainty.

The experimental investigation of decision-making in humans relies on two distinct types of paradigms, involving either description- or experience-based choices. In description-based paradigms, decision variables (i.e. payoffs and probabilities) are explicitly communicated by means of symbols. In experience-based paradigms decision variables are learnt from trial-by-trial feedback. In the decision-making literature, 'description-experience gap' refers to the fact that different biases are observed in the two experimental paradigms. Remarkably, well-documented biases of description-based choices, such as under-weighting of rare events and loss aversion, do not apply to experience-based decisions. Here, we argue that the description-experience gap represents a major challenge, not only to current decision theories, but also to the neuroeconomics research framework, which relies heavily on the translation of neurophysiological findings between human and non-human primate research. In fact, most non-human primate neurophysiological research relies on behavioural designs that share features of both description- and experience-based choices. As a consequence, it is unclear whether the neural mechanisms built from non-human primate electrophysiology should be linked to description-based or experience-based decision-making processes. The picture is further complicated by additional methodological gaps between human and non-human primate neuroscience research. After analysing these methodological challenges, we conclude proposing new lines of research to address them. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

Balancing costs and benefits in primates: ecological and palaeoanthropological views.

Maintaining the balance between costs and benefits is challenging for species living in complex and dynamic socio-ecological environments, such as primates, but also crucial for shaping life history, reproductive and feeding strategies. Indeed, individuals must decide to invest time and energy to obtain food, services and partners, with little direct feedback on the success of their investments. Whereas decision-making relies heavily upon cognition in humans, the extent to which it also involves cognition in other species, based on their environmental constraints, has remained a challenging question. Building mental representations relating behaviours and their long-term outcome could be critical for other primates, but there are actually very little data relating cognition to real socio-ecological challenges in extant and extinct primates. Here, we review available data illustrating how specific cognitive processes enable(d) modern primates and extinct hominins to manage multiple resources (e.g. food, partners) and to organize their behaviour in space and time, both at the individual and at the group level. We particularly focus on how they overcome fluctuating and competing demands, and select courses of action corresponding to the best possible packages of potential costs and benefits in reproductive and foraging contexts. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

Continuous decisions.

Humans and other animals evolved to make decisions that extend over time with continuous and ever-changing options. Nonetheless, the academic study of decision-making is mostly limited to the simple case of choice between two options. Here, we advocate that the study of choice should expand to include continuous decisions. Continuous decisions, by our definition, involve a continuum of possible responses and take place over an extended period of time during which the response is continuously subject to modification. In most continuous decisions, the range of options can fluctuate and is affected by recent responses, making consideration of reciprocal feedback between choices and the environment essential. The study of continuous decisions raises new questions, such as how abstract processes of valuation and comparison are co-implemented with action planning and execution, how we simulate the large number of possible futures our choices lead to, and how our brains employ hierarchical structure to make choices more efficiently. While microeconomic theory has proven invaluable for discrete decisions, we propose that engineering control theory may serve as a better foundation for continuous ones. And while the concept of value has proven foundational for discrete decisions, goal states and policies may prove more useful for continuous ones. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

How animals do business.

The field of comparative behavioural economics investigates decisions about the acquisition and exchange of goods and services. It does so in both humans and other species on the assumption that the cognition and emotions involved have a shared evolutionary background. This preface roughly defines the field and reviews a few selected early studies and concepts to offer a taste of what economic behaviour means in relation to species other than our own. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

Variation in primate decision-making under uncertainty and the roots of human economic behaviour.

Uncertainty is a ubiquitous component of human economic behaviour, yet people can vary in their preferences for risk across populations, individuals and different points in time. As uncertainty also characterizes many aspects of animal decision-making, comparative research can help evaluate different potential mechanisms that generate this variation, including the role of biological differences or maturational change versus cultural learning, as well as identify human-unique components of economic decision-making. Here, we examine decision-making under risk across non-human primates, our closest relatives. We first review theoretical approaches and current methods for understanding decision-making in animals. We then assess the current evidence for variation in animal preferences between species and populations, between individuals based on personality, sex and age, and finally, between different contexts and individual states. We then use these primate data to evaluate the processes that can shape human decision-making strategies and identify the primate foundations of human economic behaviour. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.