Is this worth the trouble? Strategic conflict management in Tonkean macaques.

Conflict management entails preventing and repairing damages resulting from social conflicts. While previous research has emphasized post-conflict actions like reconciliation, the understanding of how primates weigh the costs and benefits of conflict remains limited. Uncovering this hidden but fundamental aspect of conflict management requires addressing actively avoided social conflicts. In a study involving semi-free ranging Tonkean macaques, individuals were presented with social dilemmas: displacing a peer to access a preferred juice reward or opting for a peer-free but less preferred one to avoid conflict. The results showed that subjects attributed a cost to the social conflict and did not demonstrate a systematic drive to dominate. Decision modeling revealed integration of peer hierarchy and reward subjective value, with subjects' own social rank impacting the balance between these social and economic dimensions. Overall, this research highlights how primates strategically address group cohesion and peacekeeping, sometimes at the expense of personal preferences.

Spot the odd one out: do snake pictures capture macaques' attention more than other predators?

Detecting and identifying predators quickly is key to survival. According to the Snake Detection Theory (SDT), snakes have been a substantive threat to primates for millions of years, so that dedicated visual skills were tuned to detect snakes in early primates. Past experiments confronted the SDT by measuring how fast primate subjects detected snake pictures among non-dangerous distractors (e.g., flowers), but did not include pictures of primates' other predators, such as carnivorans, raptors, and crocodilians. Here, we examined the detection abilities of N = 19 Tonkean macaques (Macaca tonkeana) and N = 6 rhesus macaques (Macaca mulatta) to spot different predators. By implementing an oddity task protocol, we recorded success rates and reaction times to locate a deviant picture among four pictures over more than 400,000 test trials. Pictures depicted a predator, a non-predator animal, or a simple geometric shape. The first task consisted of detecting a deviant picture among identical distractor pictures (discrimination) and the second task was designed to evaluate detection abilities of a deviant picture among different distractor pictures (categorization). The macaques detected pictures of geometric shapes better and faster than pictures of animals, and were better and faster at discriminating than categorizing. The macaques did not detect snakes better or faster than other animal categories. Overall, these results suggest that pictures of snakes do not capture visual attention more than other predators, questioning previous findings in favor of the SDT.

Tolerant macaque species are less impulsive and reactive.

Inhibitory control, the inhibition of impulsive behaviours, is believed to be key in navigating a complex social environment. Species characterised by higher social tolerance, living in more complex groups, with more diverse relationships, face higher uncertainty regarding the outcome of social interactions and, therefore, would benefit from employing more inhibitory strategies. To date, little is known about the selective forces that favour the evolution of inhibitory control. In this study, we compared inhibitory control skills in three closely related macaque species which differ in their social tolerance style. We tested 66 macaques from two institutions (Macaca mulatta, low tolerance; M. fascicularis, medium tolerance; and M. tonkeana, high tolerance) using a battery of validated inhibitory control touchscreen tasks. Higher social tolerance was associated with enhanced inhibitory control performances. More tolerant species were less impulsive and less distracted by pictures of unknown conspecifics. Interestingly, we did not find evidence that social tolerance degree was associated with performance in reversal learning. Overall, our results support the hypothesis that evolution has promoted the development of socio-cognitive skills to cope with the demands related to the complexity of the social environment.

Orbitofrontal cortex contributes to the comparison of values underlying economic choices.

Economic choices between goods entail the computation and comparison of subjective values. Previous studies examined neuronal activity in the orbitofrontal cortex (OFC) of monkeys choosing between different types of juices. Three groups of neurons were identified: offer value cells encoding the value of individual offers, chosen juice cells encoding the identity of the chosen juice, and chosen value cells encoding the value of the chosen offer. The encoded variables capture both the input (offer value) and the output (chosen juice, chosen value) of the decision process, suggesting that values are compared within OFC. Recent work demonstrates that choices are causally linked to the activity of offer value cells. Conversely, the hypothesis that OFC contributes to value comparison has not been confirmed. Here we show that weak electrical stimulation of OFC specifically disrupts value comparison without altering offer values. This result implies that neuronal populations in OFC participate in value comparison.

Neuronal origins of reduced accuracy and biases in economic choices under sequential offers.

Economic choices are characterized by a variety of biases. Understanding their origins is a long-term goal for neuroeconomics, but progress on this front has been limited. Here, we examined choice biases observed when two goods are offered sequentially. In the experiments, rhesus monkeys chose between different juices offered simultaneously or in sequence. Choices under sequential offers were less accurate (higher variability). They were also biased in favor of the second offer (order bias) and in favor of the preferred juice (preference bias). Analysis of neuronal activity recorded in the orbitofrontal cortex revealed that these phenomena emerged at different computational stages. Lower choice accuracy reflected weaker offer value signals (valuation stage), the order bias emerged during value comparison (decision stage), and the preference bias emerged late in the trial (post-comparison). By neuronal measures, each phenomenon reduced the value obtained on average in each trial and was thus costly to the monkey.

Economic Choices under Simultaneous or Sequential Offers Rely on the Same Neural Circuit.

A series of studies in which monkeys chose between two juices offered in variable amounts identified in the orbitofrontal cortex (OFC) different groups of neurons encoding the value of individual options (offer value), the binary choice outcome (chosen juice), and the chosen value. These variables capture both the input and the output of the choice process, suggesting that the cell groups identified in OFC constitute the building blocks of a decision circuit. Several lines of evidence support this hypothesis. However, in previous experiments offers were presented simultaneously, raising the question of whether current notions generalize to when goods are presented or are examined in sequence. Recently, Ballesta and Padoa-Schioppa (2019) examined OFC activity under sequential offers. An analysis of neuronal responses across time windows revealed that a small number of cell groups encoded specific sequences of variables. These sequences appeared analogous to the variables identified under simultaneous offers, but the correspondence remained tentative. Thus, in the present study, we examined the relation between cell groups found under sequential versus simultaneous offers. We recorded from the OFC while monkeys chose between different juices. Trials with simultaneous and sequential offers were randomly interleaved in each session. We classified cells in each choice modality, and we examined the relation between the two classifications. We found a strong correspondence; in other words, the cell groups measured under simultaneous offers and under sequential offers were one and the same. This result indicates that economic choices under simultaneous or sequential offers rely on the same neural circuit.SIGNIFICANCE STATEMENT Research in the past 20 years has shed light on the neuronal underpinnings of economic choices. A large number of results indicates that decisions between goods are formed in a neural circuit within the orbitofrontal cortex. In most previous studies, subjects chose between two goods offered simultaneously. Yet, in daily situations, goods available for choice are often presented or examined in sequence. Here we recorded neuronal activity in the primate orbitofrontal cortex alternating trials under simultaneous and under sequential offers. Our analyses demonstrate that the same neural circuit supports choices in the two modalities. Hence, current notions on the neuronal mechanisms underlying economic decisions generalize to choices under sequential offers.

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.

Values encoded in orbitofrontal cortex are causally related to economic choices.

In the eighteenth century, Daniel Bernoulli, Adam Smith and Jeremy Bentham proposed that economic choices rely on the computation and comparison of subjective values1. This hypothesis continues to inform modern economic theory2 and research in behavioural economics3, but behavioural measures are ultimately not sufficient to verify the proposal4. Consistent with the hypothesis, when agents make choices, neurons in the orbitofrontal cortex (OFC) encode the subjective value of offered and chosen goods5. Value-encoding cells integrate multiple dimensions6-9, variability in the activity of each cell group correlates with variability in choices10,11 and the population dynamics suggests the formation of a decision12. However, it is unclear whether these neural processes are causally related to choices. More generally, the evidence linking economic choices to value signals in the brain13-15 remains correlational16. Here we show that neuronal activity in the OFC is causal to economic choices. We conducted two experiments using electrical stimulation in rhesus monkeys (Macaca mulatta). Low-current stimulation increased the subjective value of individual offers and thus predictably biased choices. Conversely, high-current stimulation disrupted both the computation and the comparison of subjective values, and thus increased choice variability. These results demonstrate a causal chain linking subjective values encoded in OFC to valuation and choice.

Economic Decisions through Circuit Inhibition.

Economic choices between goods are thought to rely on the orbitofrontal cortex (OFC), but the decision mechanisms remain poorly understood. To shed light on this fundamental issue, we recorded from the OFC of monkeys choosing between two juices offered sequentially. An analysis of firing rates across time windows revealed the presence of different groups of neurons similar to those previously identified under simultaneous offers. This observation suggested that economic decisions in the two modalities are formed in the same neural circuit. We then examined several hypotheses on the decision mechanisms. OFC neurons encoded good identities and values in a juice-based representation (labeled lines). Contrary to previous assessments, our data argued against the idea that decisions rely on mutual inhibition at the level of offer values. In fact, we showed that previous arguments for mutual inhibition were confounded by differences in value ranges. Instead, decisions seemed to involve mechanisms of circuit inhibition, whereby each offer value indirectly inhibited neurons encoding the opposite choice outcome. Our results reconcile a variety of previous findings and provide a general account for the neuronal underpinnings of economic choices.

Short-Term Reciprocity in Macaque's Social Decision-Making.

Primates live in complex social environments, where individuals create meaningful networks by adapting their behavior according to past experiences with others. Although free-ranging primates do show signs of reciprocity, experiments in more controlled environments have mainly failed to reproduce such social dynamics. Hence, the cognitive and neural processes allowing monkeys to reciprocate during social exchanges remains elusive. Here, pairs of long-tailed macaques (Macaca fascicularis) took turns into a social decision task involving the delivery of positive (juice reward) or negative (airpuff) outcomes. By analyzing the contingencies of one partner's past decisions on the other's future decisions, we demonstrate the presence of reciprocity, but only for the exchange of negative outcomes. Importantly, to display this decisional bias, the monkey needs to witness its partner's decisions, since non-social deliveries of the same outcome did not have such effect. Withholding of negative outcomes also predicted future social decisions, which suggest that the observed tit-for-tat strategy may not only be motivated by retaliation after receiving an airpuff but also by the gratefulness of not having received one. These results clarify the apparent dichotomy within the scientific literature of reciprocity in non-human primates and suggest that their social cognition comprise revenge and gratitude.

Social determinants of eyeblinks in adult male macaques.

Videos with rich social and emotional content elicit natural social behaviors in primates. Indeed, while watching videos of conspecifics, monkeys engage in eye contact, gaze follow, and reciprocate facial expressions. We hypothesized that the frequency and timing of eyeblinks also depends on the social signals contained in videos. We monitored the eyeblinks of four male adult macaques while they watched videos of conspecifics displaying facial expressions with direct or averted gaze. The instantaneous blink rate of all four animals decreased during videos. The temporal synchrony of blinking, however, increased in response to segments depicting appeasing or aggressive facial expressions directed at the viewer. Two of the four monkeys, who systematically reciprocated the direct gaze of the stimulus monkeys, also showed eyeblink entrainment, a temporal coordination of blinking between social partners engaged in dyadic interactions. Together, our results suggest that in macaques, as in humans, blinking depends not only on the physiological imperative to protect the eyes and spread a film of tears over the cornea, but also on several socio-emotional factors.

Effects of MDMA Injections on the Behavior of Socially-Housed Long-Tailed Macaques (Macaca fascicularis).

3,4-methylenedioxy-N-methyl amphetamine (MDMA) is one of the few known molecules to increase human and rodent prosocial behaviors. However, this effect has never been assessed on the social behavior of non-human primates. In our study, we subcutaneously injected three different doses of MDMA (1.0, 1.5 or 2.0mg/kg) to a group of three, socially housed, young male long-tailed macaques. More than 200 hours of behavioral data were recorded, during 68 behavioral sessions, by an automatic color-based video device that tracked the 3D positions of each animal and of a toy. This data was then categorized into 5 exclusive behaviors (resting, locomotion, foraging, social contact and object play). In addition, received and given social grooming was manually scored. Results show several significant dose-dependent behavioral effects. At 1.5mg/kg only, MDMA induces a significant increase in social grooming behavior, thus confirming the prosocial effect of MDMA in macaques. Additionally, at 1.5 and 2.0 mg/kg MDMA injection substantially decreases foraging behavior, which is consistent with the known anorexigenic effect of this compound. Furthermore, at 2.0 mg/kg MDMA injection induces an increase in locomotor behavior, which is also in accordance with its known stimulant property. Interestingly, MDMA injected at 1.0mg/kg increases the rate of object play, which might be interpreted as a decrease of the inhibition to manipulate a unique object in presence of others, or, as an increase of the intrinsic motivation to manipulate this object. Together, our results support the effectiveness of MDMA to study the complex neurobiology of primates' social behaviors.

Rudimentary empathy in macaques' social decision-making.

Primates live in highly social environments, where prosocial behaviors promote social bonds and cohesion and contribute to group members' fitness. Despite a growing interest in the biological basis of nonhuman primates' social interactions, their underlying motivations remain a matter of debate. We report that macaque monkeys take into account the welfare of their peers when making behavioral choices bringing about pleasant or unpleasant outcomes to a monkey partner. Two macaques took turns in making decisions that could impact their own welfare or their partner's. Most monkeys were inclined to refrain from delivering a mildly aversive airpuff and to grant juice rewards to their partner. Choice consistency between these two types of outcome suggests that monkeys display coherent motivations in different social interactions. Furthermore, spontaneous affilitative group interactions in the home environment were mostly consistent with the measured social decisions, thus emphasizing the impact of preexisting social bonds on decision-making. Interestingly, unique behavioral markers predicted these decisions: benevolence was associated with enhanced mutual gaze and empathic eye blinking, whereas indifference or malevolence was associated with lower or suppressed such responses. Together our results suggest that prosocial decision-making is sustained by an intrinsic motivation for social affiliation and controlled through positive and negative vicarious reinforcements.

Blood microsampling from the ear capillary in non-human primates.

Blood sampling from awake non-human primates (NHPs) is classically performed under constraint in the cephalic or saphenous vein. It is a challenging, potentially harmful and stressful procedure which may lead to biased results and raises ethical concerns. Laboratory NHPs undergo a head-restrained procedure allowing for a safer procedure of collecting blood from their ears. Using regular capillary blood collection devices 500 µL of blood can be easily withdrawn per puncture point, which is sufficient for performing most of the usual modern biological assays. This procedure has been validated by measuring total proteins, cortisol and vasopressin concentrations from concomitant blood samples taken from the saphenous vein and the ear capillary vessels of macaques (n = 16). We observed strong correlations between the blood concentrations of total proteins, cortisol and vasopressin (r = 0.72, r = 0.63, r = 0.83, respectively; all P values <0.01) taken from the saphenous vein and from the ear capillary. There were no significant differences between blood concentrations taken from the saphenous vein and the ear capillary. Our alternative to the classical blood collection procedure is harmless and can be routinely performed, which can therefore improve scientific results while increasing animal welfare in accordance with the 3R (replacement, reduction and refinement) principles.

Compete to play: trade-off with social contact in long-tailed macaques (Macaca fascicularis).

Many animal species engage in various forms of solitary object play, but this activity seems to be of particular importance in primates. If playing objects constitute a valuable resource, and access to such objects is limited, a competitive context may arise. We inserted a unique toy within a mini-colony of long-tailed macaque (Macaca fascicularis) and compared their behaviors to sessions without playing object. An automatic color-based 3D video device was used to track the positions of each animal and the toy, and this data was categorized into 5 exclusive behaviors (resting, locomotion, foraging, social contact and object play). As expected, the delay to first access to the object reflected the hierarchy of the colony, indicating that a competition took place to own this unique resource of entertainment. In addition, we found that the amount of object play was not correlated with social or foraging behavior, suggesting independent motivational mechanisms. Conversely, object playing time was negatively correlated with idling time, thus indicating its relation to pastime activities. Interestingly, the amount of social contacts in the group was significantly reduced by the heightened competitive context, suggesting that competitors are more likely to be perceived as potential threat requiring caution, as shown in humans. Experimental manipulation of competitive contexts in primates reveals common mental processes involved in social judgment, and shows that access to valuable resources can be a sufficient cause for variations in group cohesion.