Sociability in a non-captive macaque population is associated with beneficial gut bacteria.

The relationship between social behaviour and the microbiome is known to be reciprocal. Research in wild animal populations, particularly in primate social groups, has revealed the role that social interactions play in microbial transmission, whilst studies in laboratory animals have demonstrated that the gut microbiome can affect multiple aspects of behaviour, including social behaviour. Here we explore behavioural variation in a non-captive animal population with respect to the abundance of specific bacterial genera. Social behaviour based on grooming interactions is assessed in a population of rhesus macaques (Macaca mulatta), and combined with gut microbiome data. We focus our analyses on microbiome genera previously linked to sociability and autistic behaviours in rodents and humans. We show in this macaque population that some of these genera are also related to an individual's propensity to engage in social interactions. Interestingly, we find that several of the genera positively related to sociability, such as Faecalibacterium, are well known for their beneficial effects on health and their anti-inflammatory properties. In contrast, the genus Streptococcus, which includes pathogenic species, is more abundant in less sociable macaques. Our results indicate that microorganisms whose abundance varies with individual social behaviour also have functional links to host immune status. Overall, these findings highlight the connections between social behaviour, microbiome composition, and health in an animal population.

Limited microbiome differences in captive and semi-wild primate populations consuming similar diets.

Gut microbial communities are shaped by a myriad of extrinsic factors, including diet and the environment. Although distinct human populations consistently exhibit different gut microbiome compositions, variation in diet and environmental factors are almost always coupled, making it difficult to disentangle their relative contributions to shaping the gut microbiota. Data from discrete animal populations with similar diets can help reduce confounds. Here, we assessed the gut microbiota of free-ranging and captive rhesus macaques with at least 80% diet similarity to test the hypothesis that hosts in difference environments will have different gut microbiomes despite a shared diet. Although we found that location was a significant predictor of gut microbial composition, the magnitude of observed differences was relatively small. These patterns suggest that a shared diet may limit the typical influence of environmental microbial exposure on the gut microbiota.

Cannabis Use and Resting State Functional Connectivity in the Aging Brain.

Several lines of evidence suggest that older adults (aged 65+) sharply increased their cannabis use over the last decade, highlighting a need to understand the effects of cannabis in this age group. Pre-clinical models suggest that cannabinoids affect the brain and cognition in an age-dependent fashion, having generally beneficial effects on older animals and deleterious effects on younger ones. However, there is little research on how cannabis affects the brains of older adults or how older adults differ from younger adults who use cannabis. Resting state functional connectivity (rsFC) measures provide sensitive metrics of age-related cognitive decline. Here we compared rsFC in older adults who are either regular users of cannabis or non-users. We found stronger connectivity between sources in the hippocampus and parahippocampal cortex, and targets in the anterior lobes of the cerebellum in older adult cannabis users relative to non-users. A similar pattern of strengthened connectivity between hippocampal and cerebellar structures was also present in 25-35 year old non-users in comparison to 60-88 year old non-users. These findings suggest that future studies should examine both the potential risks of cannabinoids, as well as a potential benefits, on cognition and brain health for older adults.

Neurons in primate prefrontal cortex signal valuable social information during natural viewing.

Information about social partners is innately valuable to primates. Decisions about which sources of information to consume are highly naturalistic but also complex and place unusually strong demands on the brain's decision network. In particular, both the orbitofrontal cortex (OFC) and lateral prefrontal cortex (LPFC) play key roles in decision making and social behaviour, suggesting a likely role in social information-seeking as well. To test this idea, we developed a 'channel surfing' task in which monkeys were shown a series of 5 s video clips of conspecifics engaged in natural behaviours at a field site. Videos were annotated frame-by-frame using an ethogram of species-typical behaviours, an important source of social information. Between each clip, monkeys were presented with a choice between targets that determined which clip would be seen next. Monkeys' gaze during playback indicated differential engagement depending on what behaviours were presented. Neurons in both OFC and LPFC responded to choice targets and to video, and discriminated a subset of the behaviours in the ethogram during video viewing. These findings suggest that both OFC and LPFC are engaged in processing social information that is used to guide dynamic information-seeking decisions. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

Correction: Rhesus macaques form preferences for brand logos through sex and social status based advertising.

[This corrects the article DOI: 10.1371/journal.pone.0193055.].

Neurobiology of social reward valuation in adults with a history of anorexia nervosa.

OBJECTIVE: Anorexia nervosa (AN) is a disorder characterized by atypical patterns of reward valuation (e.g. positive valuation of hunger). Atypical reward processing may extend into social domains. If so, such findings would be of prognostic significance as impaired social functioning predicts worse outcome. We explore neural circuits implicated in social reward processing in individuals with a history of AN who are weight-restored relative to controls and examine the effects of illness course on the experience of social value. METHOD: 20 weight-restored individuals with a history of AN (AN-WR) and 24 healthy control (HC) participants were assessed using fMRI tasks that tapped social reward: smiling faces and full human figures that varied in attractiveness and weight. RESULTS: AN-WR differed from HC in attractiveness ratings by weight (negatively correlated in AN-WR). While there were no significant differences when viewing smiling faces, viewing full figures resulted in decreased activation in regions implicated in reward valuation (the right caudate) for AN-WR and this region was negatively correlated with a sustained course of the disorder. Exploratory whole brain analyses revealed reduced activation in regions associated with social reward, self-referential processing, and cognitive reappraisal (e.g., medial prefrontal cortex, striatum, and nucleus accumbens) with sustained disorder course. DISCUSSION: The rewarding value of full body images decreases with a sustained disorder course. This may reflect an extension of atypical reward processing documented in AN-WR, perhaps as a function of starvation dampening visceral motivational signals; the deployment of cognitive strategies that lessen the experience of reward; and/or the nature of the stimuli themselves as provocative of eating disorder symptoms (e.g., thin bodies). These findings did not extend to smiling face stimuli. Advances in technology (e.g., virtual avatars, text messaging) may provide novel means to build relationships, including therapeutic relationships, to support improved social connections without threats to symptom provocation.

Rhesus macaques form preferences for brand logos through sex and social status based advertising.

Like humans, monkeys value information about sex and status, inviting the hypothesis that our susceptibility to these factors in advertising arises from shared, ancestral biological mechanisms that prioritize social information. To test this idea, we asked whether rhesus macaques (Macaca mulatta) show choice behavior that is similar to humans in response to sex and social status in advertising. Our results show that monkeys form preferences for brand logos repeatedly paired with images of macaque genitals and high status monkeys. Moreover, monkeys sustain preferences for these brand logos even though choosing them provided no tangible rewards, a finding that cannot be explained by a decision mechanism operating solely on material outcomes. Together, our results endorse the hypothesis that the power of sex and status in advertising emerges from the spontaneous engagement of shared, ancestral neural circuits that prioritize information useful for navigating the social environment. Finally, our results show that simple associative conditioning is sufficient to explain the formation of preferences for brand logos paired with sexual or status-based images.

Increased reward value of non-social stimuli in children and adolescents with autism.

An econometric choice task was used to estimate the implicit reward value of social and non-social stimuli related to restricted interests in children and adolescents with (n = 12) and without (n = 22) autism spectrum disorder (ASD). Mixed effects logistic regression analyses revealed that groups differed in valuation of images related to restricted interests: control children were indifferent to cash payouts to view these images, but children with ASD were willing to receive less cash payout to view these images. Groups did not differ in valuation of social images or non-social images not related to restricted interests. Results highlight that motivational accounts of ASD should also consider the reward value of non-social stimuli related to restricted interests in ASD (Dichter and Adolphs, 2012).

Decision making: the neuroethological turn.

Neuroeconomics applies models from economics and psychology to inform neurobiological studies of choice. This approach has revealed neural signatures of concepts like value, risk, and ambiguity, which are known to influence decision making. Such observations have led theorists to hypothesize a single, unified decision process that mediates choice behavior via a common neural currency for outcomes like food, money, or social praise. In parallel, recent neuroethological studies of decision making have focused on natural behaviors like foraging, mate choice, and social interactions. These decisions strongly impact evolutionary fitness and thus are likely to have played a key role in shaping the neural circuits that mediate decision making. This approach has revealed a suite of computational motifs that appear to be shared across a wide variety of organisms. We argue that the existence of deep homologies in the neural circuits mediating choice may have profound implications for understanding human decision making in health and disease.

Social learning in humans and other animals.

Decisions made by individuals can be influenced by what others think and do. Social learning includes a wide array of behaviors such as imitation, observational learning of novel foraging techniques, peer or parental influences on individual preferences, as well as outright teaching. These processes are believed to underlie an important part of cultural variation among human populations and may also explain intraspecific variation in behavior between geographically distinct populations of animals. Recent neurobiological studies have begun to uncover the neural basis of social learning. Here we review experimental evidence from the past few decades showing that social learning is a widespread set of skills present in multiple animal species. In mammals, the temporoparietal junction, the dorsomedial, and dorsolateral prefrontal cortex, as well as the anterior cingulate gyrus, appear to play critical roles in social learning. Birds, fish, and insects also learn from others, but the underlying neural mechanisms remain poorly understood. We discuss the evolutionary implications of these findings and highlight the importance of emerging animal models that permit precise modification of neural circuit function for elucidating the neural basis of social learning.

Individual differences in social information gathering revealed through Bayesian hierarchical models.

As studies of the neural circuits underlying choice expand to include more complicated behaviors, analysis of behaviors elicited in laboratory paradigms has grown increasingly difficult. Social behaviors present a particular challenge, since inter- and intra-individual variation are expected to play key roles. However, due to limitations on data collection, studies must often choose between pooling data across all subjects or using individual subjects' data in isolation. Hierarchical models mediate between these two extremes by modeling individual subjects as drawn from a population distribution, allowing the population at large to serve as prior information about individuals' behavior. Here, we apply this method to data collected across multiple experimental sessions from a set of rhesus macaques performing a social information valuation task. We show that, while the values of social images vary markedly between individuals and between experimental sessions for the same individual, individuals also differentially value particular categories of social images. Furthermore, we demonstrate covariance between values for image categories within individuals and find evidence suggesting that magnitudes of stimulus values tend to diminish over time.

Oxytocin blunts social vigilance in the rhesus macaque.

Exogenous application of the neuromodulatory hormone oxytocin (OT) promotes prosocial behavior and can improve social function. It is unclear, however, whether OT promotes prosocial behavior per se, or whether it facilitates social interaction by reducing a state of vigilance toward potential social threats. To disambiguate these two possibilities, we exogenously delivered OT to male rhesus macaques, which have a characteristic pattern of species-typical social vigilance, and examined their performance in three social attention tasks. We first determined that, in the absence of competing task demands or goals, OT increased attention to faces and eyes, as in humans. By contrast, OT reduced species typical social vigilance for unfamiliar, dominant, and emotional faces in two additional tasks. OT eliminated the emergence of a typical state of vigilance when dominant face images were available during a social image choice task. Moreover, OT improved performance on a reward-guided saccade task, despite salient social distractors: OT reduced the interference of unfamiliar faces, particularly emotional ones, when these faces were task irrelevant. Together, these results demonstrate that OT suppresses vigilance toward potential social threats in the rhesus macaque. We hypothesize that a basic role for OT in regulating social vigilance may have facilitated the evolution of prosocial behaviors in humans.

Neuroethology of primate social behavior.

A neuroethological approach to human and nonhuman primate behavior and cognition predicts biological specializations for social life. Evidence reviewed here indicates that ancestral mechanisms are often duplicated, repurposed, and differentially regulated to support social behavior. Focusing on recent research from nonhuman primates, we describe how the primate brain might implement social functions by coopting and extending preexisting mechanisms that previously supported nonsocial functions. This approach reveals that highly specialized mechanisms have evolved to decipher the immediate social context, and parallel circuits have evolved to translate social perceptual signals and nonsocial perceptual signals into partially integrated social and nonsocial motivational signals, which together inform general-purpose mechanisms that command behavior. Differences in social behavior between species, as well as between individuals within a species, result in part from neuromodulatory regulation of these neural circuits, which itself appears to be under partial genetic control. Ultimately, intraspecific variation in social behavior has differential fitness consequences, providing fundamental building blocks of natural selection. Our review suggests that the neuroethological approach to primate behavior may provide unique insights into human psychopathology.

Social signals in primate orbitofrontal cortex.

Primate evolution produced an increased capacity to respond flexibly to varying social contexts as well as expansion of the prefrontal cortex. Despite this association, how prefrontal neurons respond to social information remains virtually unknown. People with damage to their orbitofrontal cortex (OFC) struggle to recognize facial expressions, make poor social judgments, and frequently make social faux pas. Here we test explicitly whether neurons in primate OFC signal social information and, if so, how such signals compare with responses to primary fluid rewards. We find that OFC neurons distinguish images that belong to socially defined categories, such as female perinea and faces, as well as the social dominance of those faces. These modulations signaled both how much monkeys valued these pictures and their interest in continuing to view them. Far more neurons signaled social category than signaled fluid value, despite the stronger impact of fluid reward on monkeys' choices. These findings indicate that OFC represents both the motivational value and attentional priority of other individuals, thus contributing to both the acquisition of information about others and subsequent social decisions. Our results betray a fundamental disconnect between preferences expressed through overt choice, which were primarily driven by the desire for more fluid, and preferential neuronal processing, which favored social computations.

Of mice and monkeys: using non-human primate models to bridge mouse- and human-based investigations of autism spectrum disorders.

The autism spectrum disorders (ASDs) arise from a diverse array of genetic and environmental origins that disrupt the typical developmental trajectory of neural connectivity and synaptogenesis. ASDs are marked by dysfunctional social behavior and cognition, among other deficits. Greater understanding of the biological substrates of typical social behavior in animal models will further our understanding of the etiology of ASDs. Despite the precision and tractability of molecular genetics models of ASDs in rodents, these organisms lack the complexity of human social behavior, thus limiting their impact on understanding ASDs to basic mechanisms. Non-human primates (NHPs) provide an attractive, complementary model for ASDs, due in part to the complexity and dynamics of social structures, reliance on vision for social signaling, and deep homology in brain circuitry mediating social behavior and reward. This knowledge is based on a rich literature, compiled over 50 years of observing primate behavior in the wild, which, in the case of rhesus macaques, is complemented by a large body of research characterizing neuronal activity during cognitive behavior. Several recent developments in this field are directly relevant to ASDs, including how the brain represents the perceptual features of social stimuli, how social information influences attention processes in the brain, and how the value of social interaction is computed. Because the symptoms of ASDs may represent extreme manifestations of traits that vary in intensity within the general population, we will additionally discuss ways in which nonhuman primates also show variation in social behavior and reward sensitivity. In cases where variation in species-typical behavior is analogous to similar variations in human behavior, we believe that study of the neural circuitry underlying this variation will provide important insights into the systems-level mechanisms contributing to ASD pathology.

Neuroethology of decision-making.

A neuroethological approach to decision-making considers the effect of evolutionary pressures on neural circuits mediating choice. In this view, decision systems are expected to enhance fitness with respect to the local environment, and particularly efficient solutions to specific problems should be conserved, expanded, and repurposed to solve other problems. Here, we discuss basic prerequisites for a variety of decision systems from this viewpoint. We focus on two of the best-studied and most widely represented decision problems. First, we examine patch leaving, a prototype of environmentally based switching between action patterns. Second, we consider social information seeking, a process resembling foraging with search costs. We argue that while the specific neural solutions to these problems sometimes differ across species, both the problems themselves and the algorithms instantiated by biological hardware are repeated widely throughout nature. The behavioral and mathematical study of ubiquitous decision processes like patch leaving and social information seeking thus provides a powerful new approach to uncovering the fundamental design structure of nervous systems.

Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus macaques (Macaca mulatta).

People attend not only to their own experiences, but also to the experiences of those around them. Such social awareness profoundly influences human behavior by enabling observational learning, as well as by motivating cooperation, charity, empathy, and spite. Oxytocin (OT), a neurosecretory hormone synthesized by hypothalamic neurons in the mammalian brain, can enhance affiliation or boost exclusion in different species in distinct contexts, belying any simple mechanistic neural model. Here we show that inhaled OT penetrates the CNS and subsequently enhances the sensitivity of rhesus macaques to rewards occurring to others as well as themselves. Roughly 2 h after inhaling OT, monkeys increased the frequency of prosocial choices associated with reward to another monkey when the alternative was to reward no one. OT also increased attention to the recipient monkey as well as the time it took to render such a decision. In contrast, within the first 2 h following inhalation, OT increased selfish choices associated with delivery of reward to self over a reward to the other monkey, without affecting attention or decision latency. Despite the differences in species typical social behavior, exogenous, inhaled OT causally promotes social donation behavior in rhesus monkeys, as it does in more egalitarian and monogamous ones, like prairie voles and humans, when there is no perceived cost to self. These findings potentially implicate shared neural mechanisms.

Visual preferences for sex and status in female rhesus macaques.

Most primates are both highly visual and highly social. These qualities predict that visual cues to social variables, such as identity, sex, social status, and reproductive quality, would be intrinsically valuable and systematically attract attention. Supporting this idea, thirsty male rhesus macaques (Macaca mulatta) will forego fluid reward to view images of the faces of high-ranking males and the sexual skin of females. Whether female rhesus macaques, who experience dramatically different social pressures and reproductive costs than male macaques, also systematically and spontaneously value visual cues to social information remains untested experimentally. We probed the preferences of female rhesus macaques, given the opportunity to display an image from a known class of social stimuli or touch a second target to display a blank screen. We found that females preferred faces of high-status males and also images of the perinea of both males and females, but were not motivated to display images of subordinate males or control stimuli. These findings endorse the view that both male and female rhesus macaques-and presumably other highly social primates-seek information about other individuals in a way that matches the adaptive value of that information for guiding social behavior.

Altered social reward and attention in anorexia nervosa.

Dysfunctional social reward and social attention are present in a variety of neuropsychiatric disorders including autism, schizophrenia, and social anxiety. Here we show that similar social reward and attention dysfunction are present in anorexia nervosa (AN), a disorder defined by avoidance of food and extreme weight loss. We measured the implicit reward value of social stimuli for female participants with (n = 11) and without (n = 11) AN using an econometric choice task and also tracked gaze patterns during free viewing of images of female faces and bodies. As predicted, the reward value of viewing bodies varied inversely with observed body weight for women with anorexia but not control women, in contrast with their explicit ratings of attractiveness. Surprisingly, women with AN, unlike control women, did not find female faces rewarding and avoided looking at both the face and eyes - independent of observed body weight. These findings suggest comorbid dysfunction in the neural circuits mediating gustatory and social reward in anorexia nervosa.

Serotonin transporter genotype modulates social reward and punishment in rhesus macaques.

BACKGROUND: Serotonin signaling influences social behavior in both human and nonhuman primates. In humans, variation upstream of the promoter region of the serotonin transporter gene (5-HTTLPR) has recently been shown to influence both behavioral measures of social anxiety and amygdala response to social threats. Here we show that length polymorphisms in 5-HTTLPR predict social reward and punishment in rhesus macaques, a species in which 5-HTTLPR variation is analogous to that of humans. METHODOLOGY/PRINCIPAL FINDINGS: In contrast to monkeys with two copies of the long allele (L/L), monkeys with one copy of the short allele of this gene (S/L) spent less time gazing at face than non-face images, less time looking in the eye region of faces, and had larger pupil diameters when gazing at photos of a high versus low status male macaques. Moreover, in a novel primed gambling task, presentation of photos of high status male macaques promoted risk-aversion in S/L monkeys but promoted risk-seeking in L/L monkeys. Finally, as measured by a "pay-per-view" task, S/L monkeys required juice payment to view photos of high status males, whereas L/L monkeys sacrificed fluid to see the same photos. CONCLUSIONS/SIGNIFICANCE: These data indicate that genetic variation in serotonin function contributes to social reward and punishment in rhesus macaques, and thus shapes social behavior in humans and rhesus macaques alike.