Describing behavioral states using a system model of the primate brain.

A system model of the primate neocortex is presented, based mainly on the neuroanatomy of the rhesus macaque monkey and consisting of a set of processing modules arranged as a perception-action hierarchy. These modules correspond to regions of the neocortex and their connectivity to that of the neocortex. A computational approach based on predicate logic is explained, and the results of a computer implementation of the model are reported, which demonstrate social behaviors involving affiliation and social conflict. The behavioral states of primates involved in these behaviors can be represented by the states of the system model, which have a logical representation and a diagrammatic form. It is shown how the behavioral states in goal-directed behaviors can be represented and also their short term moment-to-moment development in time. It is then shown how the state of social interaction among two or more primates can be represented, using their individual behavioral states, with interindividual action and perception. The causal dynamics of behavioral states is explained and also a control mechanism, namely, the use of confirmation signals, which stabilizes behavioral states and their dynamics. Stabilized behavioral states are seen as corresponding to coherent activations of the system, resulting from successful selection of module activations and intermodule communication with confirmation.     

Ranking network of a captive rhesus macaque society: a sophisticated corporative kingdom

We develop a three-step computing approach to explore a hierarchical ranking network for a society of captive rhesus macaques. The computed network is sufficiently informative to address the question: Is the ranking network for a rhesus macaque society more like a kingdom or a corporation? Our computations are based on a three-step approach. These steps are devised to deal with the tremendous challenges stemming from the transitivity of dominance as a necessary constraint on the ranking relations among all individual macaques, and the very high sampling heterogeneity in the behavioral conflict data. The first step simultaneously infers the ranking potentials among all network members, which requires accommodation of heterogeneous measurement error inherent in behavioral data. Our second step estimates the social rank for all individuals by minimizing the network-wide errors in the ranking potentials. The third step provides a way to compute confidence bounds for selected empirical features in the social ranking. We apply this approach to two sets of conflict data pertaining to two captive societies of adult rhesus macaques. The resultant ranking network for each society is found to be a sophisticated mixture of both a kingdom and a corporation. Also, for validation purposes, we reanalyze conflict data from twenty longhorn sheep and demonstrate that our three-step approach is capable of correctly computing a ranking network by eliminating all ranking error.     

Network stability is a balancing act of personality, power, and conflict dynamics in rhesus macaque societies

Stability in biological systems requires evolved mechanisms that promote robustness. Cohesive primate social groups represent one example of a stable biological system, which persist in spite of frequent conflict. Multiple sources of stability likely exist for any biological system and such robustness, or lack thereof, should be reflected and thus detectable in the group's network structure, and likely at multiple levels. Here we show how network structure and group stability are linked to the fundamental characteristics of the individual agents in groups and to the environmental and social contexts in which these individuals interact. Both internal factors (e.g., personality, sex) and external factors (e.g., rank dynamics, sex ratio) were considered from the level of the individual to that of the group to examine the effects of network structure on group stability in a nonhuman primate species. The results yielded three main findings. First, successful third-party intervention behavior is a mechanism of group stability in rhesus macaques in that successful interventions resulted in less wounding in social groups. Second, personality is the primary factor that determines which individuals perform the role of key intervener, via its effect on social power and dominance discrepancy. Finally, individuals with high social power are not only key interveners but also key players in grooming networks and receive reconciliations from a higher diversity of individuals. The results from this study provide sound evidence that individual and group characteristics such as personality and sex ratio influence network structures such as patterns of reconciliation, grooming and conflict intervention that are indicators of network robustness and consequent health and well-being in rhesus macaque societies. Utilizing this network approach has provided greater insight into how behavioral and social processes influence social stability in nonhuman primate groups.     

基于团抱行为的太行山猕猴社会联属

社会联属是指一些社会性动物社群内由于不同年龄、性别组的个体的社会角色与等级地位存在明显差异,在个体间形成的复杂的支配-从属关系,而这种支配-从属关系在不同的物种有着各自独特的模式(Clutton-Brock,1974)。了解社群内个体通过亲缘、非亲缘联盟、婚配、竞争而建立的支配-从属关系,是进一步开展社群内个体等级与资源竞争、互惠利益、母系投入策略等诸多研究的前提,     

Staging Social Structures: Ritual and Social Organisation in an Egalitarian Society. The Pastoral Pokot of Northern Kenya

The pastoral Pokot of northern Kenya represent their society as highly structured by descent and age grading. Descent groups (clans, lineages) and age grades (age sets, generation sets) are depicted as bounded but related units within a complex hierarchical and coherent system, the essence of Pokot society which is staged and visualised in major rituals. This study shows that they are not important in Pokot economic exchange. The formal analysis of livestock exchange networks centred upon individuals shows that emic representations do not match actual exchange behaviour. Complementing the well-established structuralist representation of pastoral social systems, this paper investigates the agency aspect, which has been largely unexplored. It furthermore documents how social exchange is contained in the various institutions of descent and age grading. Contextualising the case historically it is shown that the pastoral Pokot developed from a fragmented clan-based agro-pastoral society in which descent was the main ordering principle for land tenure and conflict management into a more comprehensive social entity with clearly definable borders to the outside, dense internal exchange networks and strong representations of the corporateness of subgroups. The rapid adoption of mobile livestock husbandry was accompanied by the rise of widespread exchange networks and social interaction with a much wider group of unrelated actors marking the foundations of a pastoral society.     

Social interaction in synthetic and natural microbial communities

Social interaction among cells is essential for multicellular complexity. But how do molecular networks within individual cells confer the ability to interact? And how do those same networks evolve from the evolutionary conflict between individual‐ and population‐level interests? Recent studies have dissected social interaction at the molecular level by analyzing both synthetic and natural microbial populations. These studies shed new light on the role of population structure for the evolution of cooperative interactions and revealed novel molecular mechanisms that stabilize cooperation among cells. New understanding of populations is changing our view of microbial processes, such as pathogenesis and antibiotic resistance, and suggests new ways to fight infection by exploiting social interaction. The study of social interaction is also challenging established paradigms in cancer evolution and immune system dynamics. Finding similar patterns in such diverse systems suggests that the same ‘social interaction motifs’ may be general to many cell populations.     

Interspecies pair housing of macaques in a research facility

The eighth edition of The Guide for the Care and Use of Laboratory Animals establishes social housing as the 'default' for social species including non-human primates. The advantages of social housing for primates have been well established, but small research facilities housing few primates in indoor cages have struggled with social housing as a result of limitations on appropriate housing and availability of compatible monkeys. Here, we report a novel approach to pair housing macaques - crossing species. We have successfully pair housed an intact male rhesus macaque with an intact male cynomolgus macaque, and an adult female rhesus macaque with numerous subadult female cynomolgus macaques. Monkeys in these pairs established dominant-subordinate relationships similar to same-species pairs. Rhesus and cynomolgus macaques can be successfully paired for the purpose of social housing in facilities with limited numbers of monkeys.     

Social behavior in aged rhesus macaques

This study investigated the relationship between chronological age and social behavior in 42 adult male and female rhesus macaques (Macaca mulatta) in three specific areas: social interactions, social roles, and social networks. While both old males and old females share behavioral differences associated with senescence, this study reports that old females and old males are distinct in their social behaviors, both from each other and from other adults. Many of these differences appear progressive across age classes, e.g., declining across age classes in females and increasing across age classes in males. Old females are less social and have smaller social networks than other females, while the opposite was found to be true of old males. An explanation for the sex-based differences in aged social behavior and social networks reported in this study may originate in rhesus matrifocal social structure.     

A Novel Experimental and Analytical Approach to the Multimodal Neural Decoding of Intent During Social Interaction in Freely-behaving Human Infants

Understanding typical and atypical development remains one of the fundamental questions in developmental human neuroscience. Traditionally, experimental paradigms and analysis tools have been limited to constrained laboratory tasks and contexts due to technical limitations imposed by the available set of measuring and analysis techniques and the age of the subjects. These limitations severely limit the study of developmental neural dynamics and associated neural networks engaged in cognition, perception and action in infants performing “in action and in context”. This protocol presents a novel approach to study infants and young children as they freely organize their own behavior, and its consequences in a complex, partly unpredictable and highly dynamic environment. The proposed methodology integrates synchronized high-density active scalp electroencephalography (EEG), inertial measurement units (IMUs), video recording and behavioral analysis to capture brain activity and movement non-invasively in freely-behaving infants. This setup allows for the study of neural network dynamics in the developing brain, in action and context, as these networks are recruited during goal-oriented, exploration and social interaction tasks.     

Face Patch Resting State Networks Link Face Processing to Social Cognition

Faces transmit a wealth of social information. How this information is exchanged between face-processing centers and brain areas supporting social cognition remains largely unclear. Here we identify these routes using resting state functional magnetic resonance imaging in macaque monkeys. We find that face areas functionally connect to specific regions within frontal, temporal, and parietal cortices, as well as subcortical structures supporting emotive, mnemonic, and cognitive functions. This establishes the existence of an extended face-recognition system in the macaque. Furthermore, the face patch resting state networks and the default mode network in monkeys show a pattern of overlap akin to that between the social brain and the default mode network in humans: this overlap specifically includes the posterior superior temporal sulcus, medial parietal, and dorsomedial prefrontal cortex, areas supporting high-level social cognition in humans. Together, these results reveal the embedding of face areas into larger brain networks and suggest that the resting state networks of the face patch system offer a new, easily accessible venue into the functional organization of the social brain and into the evolution of possibly uniquely human social skills.     

Assessing Social Engagement in Heterogeneous Groups of Zebrafish: A New Paradigm for Autism-Like Behavioral Responses

Because of its highly developed social character, zebrafish is a promising model system for the study of the genetic and neurochemical basis of altered social engagement such as is common in autism and schizophrenia. The traditional shoaling paradigm investigates social cohesion in homogeneous groups of zebrafish. However, the social dynamics of mixed groups is gaining interest from a therapeutic point of view and thus warrants animal modeling. Furthermore, mutant zebrafish are not always available in large numbers. Therefore, we developed a new paradigm that allows exploring shoaling in heterogeneous groups. The effects of MK-801, a non-competitive antagonist of the glutamate N-methyl-D-aspartate (NMDA) receptor, on social cohesion were studied to evaluate the paradigm. The drug has previously been shown to mimic aspects of autism and schizophrenia. Our results show that a single MK-801-treated zebrafish reduced social cohesion of the entire shoal drastically. Preliminary observations suggest that the social dynamics of the shoal as a whole was altered.     

Social Contact Following Severe Aggression in Rhesus Macaques (Macaca mulatta): A New Test of the Consolation Hypothesis

Previous studies on macaque species revealed no evidence of consolation: affiliative contact between the loser of an aggressive interaction and a third party. However, typically, the researchers used short observation periods and latency to make first affiliative contact as a dependent measure. Based on social stress buffering literature, I predicted that by employing longer observation periods and percentage of time in affiliative contact as a dependent measure, I would be more likely to detect increases in affiliative contact following aggression. I observed adult female rhesus macaques for 1 hr after they received severe aggression and for 1 hr after some affiliative contact, and measured time spent in affiliative contact using instantaneous recording at 30-sec intervals. Contrary to prediction, victims of attack did not spend a greater percentage of time in affiliative contact postaggression as compared to postaffiliation. Subjects were also less likely to initiate contact with other individuals and were more likely to have contact with individuals that were dominant to their aggressor, following aggression. These results provide converging evidence that affiliative contact is not increased following aggression in macaques. I discuss the failure to bear out the predictions based on the social stress buffering literature in terms of rhesus social dynamics, the nature of aggression as a stressor, and possible mechanisms for the social stress buffering effect.     

Trophic interaction modifications: an empirical and theoretical framework

Consumer–resource interactions are often influenced by other species in the community. At present these ‘trophic interaction modifications’ are rarely included in ecological models despite demonstrations that they can drive system dynamics. Here, we advocate and extend an approach that has the potential to unite and represent this key group of non‐trophic interactions by emphasising the change to trophic interactions induced by modifying species. We highlight the opportunities this approach brings in comparison to frameworks that coerce trophic interaction modifications into pairwise relationships. To establish common frames of reference and explore the value of the approach, we set out a range of metrics for the ‘strength’ of an interaction modification which incorporate increasing levels of contextual information about the system. Through demonstrations in three‐species model systems, we establish that these metrics capture complimentary aspects of interaction modifications. We show how the approach can be used in a range of empirical contexts; we identify as specific gaps in current understanding experiments with multiple levels of modifier species and the distributions of modifications in networks. The trophic interaction modification approach we propose can motivate and unite empirical and theoretical studies of system dynamics, providing a route to confront ecological complexity.     

短尾猴的社会行为与社会关系

群体生活的动物通过社会行为相联系,社会行为的类别和发生的频率决定了动物社会关系的性质,进而决定了社会结构的类型。本文根据作者在安徽黄山对短尾猴16年的观察研究,描述和分析了一些重要的社会行为,探讨了短尾猴社会中各种社会关系的特点和性质。雌性短尾猴之间的行为比较简单,缺乏多样性,主要通过近距及理毛等状态性行为建立和维持,是长久和稳固的关系;雄性短尾猴之间具有丰富的行为,事件性行为(如拥抱、爬跨等)占主要部分,易发生冲突但也易于和解;雄性和雌性关系与繁殖季节有关,交配期主要是性关系,产仔期主要是友好关系;成体和幼体的关系主要是照料与被照料的关系。     

Measuring Information-Transfer Delays

In complex networks such as gene networks, traffic systems or brain circuits it is important to understand how long it takes for the different parts of the network to effectively influence one another. In the brain, for example, axonal delays between brain areas can amount to several tens of milliseconds, adding an intrinsic component to any timing-based processing of information. Inferring neural interaction delays is thus needed to interpret the information transfer revealed by any analysis of directed interactions across brain structures. However, a robust estimation of interaction delays from neural activity faces several challenges if modeling assumptions on interaction mechanisms are wrong or cannot be made. Here, we propose a robust estimator for neuronal interaction delays rooted in an information-theoretic framework, which allows a model-free exploration of interactions. In particular, we extend transfer entropy to account for delayed source-target interactions, while crucially retaining the conditioning on the embedded target state at the immediately previous time step. We prove that this particular extension is indeed guaranteed to identify interaction delays between two coupled systems and is the only relevant option in keeping with Wiener’s principle of causality. We demonstrate the performance of our approach in detecting interaction delays on finite data by numerical simulations of stochastic and deterministic processes, as well as on local field potential recordings. We also show the ability of the extended transfer entropy to detect the presence of multiple delays, as well as feedback loops. While evaluated on neuroscience data, we expect the estimator to be useful in other fields dealing with network dynamics.     

Reflexive social attention in monkeys and humans

For humans, social cues often guide the focus of attention. Although many nonhuman primates, like humans, live in large, complex social groups, the extent to which human and nonhuman primates share fundamental mechanisms of social attention remains unexplored. Here, we show that, when viewing a rhesus macaque looking in a particular direction, both rhesus macaques and humans reflexively and covertly orient their attention in the same direction. Specifically, when performing a peripheral visual target detection task, viewing a monkey with either its eyes alone or with both its head and eyes averted to one side facilitated the detection of peripheral targets when they randomly appeared on the same side. Moreover, viewing images of a monkey with averted gaze evoked small but systematic shifts in eye position in the direction of gaze in the image. The similar magnitude and temporal dynamics of response facilitation and eye deviation in monkeys and humans suggest shared neural circuitry mediating social attention.     

Beyond Contagion: Reality Mining Reveals Complex Patterns of Social Influence

Contagion, a concept from epidemiology, has long been used to characterize social influence on people’s behavior and affective (emotional) states. While it has revealed many useful insights, it is not clear whether the contagion metaphor is sufficient to fully characterize the complex dynamics of psychological states in a social context. Using wearable sensors that capture daily face-to-face interaction, combined with three daily experience sampling surveys, we collected the most comprehensive data set of personality and emotion dynamics of an entire community of work. From this high-resolution data about actual (rather than self-reported) face-to-face interaction, a complex picture emerges where contagion (that can be seen as adaptation of behavioral responses to the behavior of other people) cannot fully capture the dynamics of transitory states. We found that social influence has two opposing effects on states: adaptation effects that go beyond mere contagion, and complementarity effects whereby individuals’ behaviors tend to complement the behaviors of others. Surprisingly, these effects can exhibit completely different directions depending on the stable personality or emotional dispositions (stable traits) of target individuals. Our findings provide a foundation for richer models of social dynamics, and have implications on organizational engineering and workplace well-being.     

Whole-genome sequencing and analysis of the Malaysian cynomolgus macaque (Macaca fascicularis) genome

ABSTRACT: BACKGROUND: The genetic background of the cynomolgus macaque (Macaca fascicularis) is made complex by the high genetic diversity, population structure, and gene introgression from the closely related rhesus macaque (Macaca mulatta). Herein we report the whole-genome sequence of a Malaysian cynomolgus macaque male with more than 40-fold coverage, which was determined using a resequencing method based on the Indian rhesus macaque genome. RESULTS: We identified approximately 9.7 million single nucleotide variants (SNVs) between the Malaysian cynomolgus and the Indian rhesus macaque genomes. Compared with humans, a smaller nonsynonymous/synonymous SNV ratio in the cynomolgus macaque suggests more effective removal of slightly deleterious mutations. Comparison of two cynomolgus (Malaysian and Vietnamese) and two rhesus (Indian and Chinese) macaque genomes, including previously published macaque genomes, suggests that Indochinese cynomolgus macaques have been more affected by gene introgression from rhesus macaques. We further identified 60 nonsynonymous SNVs that completely differentiated the cynomolgus and rhesus macaque genomes, and that could be important candidate variants for determining species-specific responses to drugs and pathogens. The demographic inference using the genome sequence data revealed that Malaysian cynomolgus macaques have experienced at least three population bottlenecks. CONCLUSIONS: This list of whole-genome SNVs will be useful for many future applications, such as an array-based genotyping system for macaque individuals. High-quality whole-genome sequencing of the cynomolgus macaque genome may aid studies on finding genetic differences that are responsible for phenotypic diversity in macaques and may help control genetic backgrounds among individuals.     

Social Relationships in Free-Ranging Male Macaca arctoides

Macaque social relationships differ greatly between species. Based on captive studies that focus mainly on females, researchers have classified stumptail macaque (Macaca arctoides) social relationships as tolerant, as indicated by a high rate of affiliation, frequent aggression, and symmetrical conflicts. To accumulate more data on male social relationships, which are relatively understudied, and to generate comparative data, we investigated male social relationships in a provisioned group of 68 free-ranging, naturally dispersing stumptail macaques in southern Thailand. We collected continuous focal animal and ad libitum data on 7 adult and 2 subadult males, recording social behavior during 283 contact hours between December 2006 and March 2007. Stumptail macaques of this population were less tolerant than predicted based on previous studies on captive groups: Rates of spatial proximity, affiliation, and aggression were low, most males directed affiliative behavior toward higher-ranking males, and conflicts were generally of low intensity and relatively asymmetrical. Thus, male stumptail macaques of the focal group appear to differ in their social style from a previous study of a captive group that mainly comprised of females. In some traits, they are even more intolerant than rhesus macaques, an intensively studied intolerant macaque species. We also compare our data on stumptail macaque males to those on other male macaques, but available data are too sparse to draw final conclusions.