The neurobiology of social decision-making

Humans live in highly complex social environments and some of our most important decisions are made in the context of social interactions. Research that probes the neural basis of decision-making in the context of social interactions combines behavioral paradigms from game theory with a variety of methods from neuroscience. The neural correlates of decision making in reciprocal exchange and bargaining games have been probed with functional neuroimaging, transcranial magnetic stimulation, and pharmacological manipulations. These studies have begun to elucidate a set of brain regions and neurotransmitter systems involved in decision-making in social interactions.     

Toward understanding how early-life social experiences alter oxytocin- and vasopressin-regulated social behaviors

The early-life social environment has profound effects on brain development and subsequent expression of social behavior. Oxytocin and vasopressin are expressed and released in the brain and are important regulators of social behavior. Accordingly, the early social environment may alter social behaviors via changes in the oxytocin and/or vasopressin systems. To test this hypothesis, and to gain mechanistic insights, rodent models mimicking either a deprived (e.g. maternal separation) or enriched (e.g. neonatal handling) early social environment have been utilized. Findings indeed show that differences in the quality of the early social environment are associated with brain region-specific alterations in oxytocin and vasopressin expression and oxytocin receptor and vasopressin 1a receptor binding. Early social environment-induced changes in oxytocin and vasopressin systems were associated with changes in several forms of social behavior, including maternal care, aggression, play-fighting, and social recognition. First studies provide evidence for a causal link between altered vasopressin responsiveness and impairments in social recognition in rats exposed to maternal separation and a role for epigenetic mechanisms to explain persistent increases in vasopressin expression in mice exposed to maternal separation. Overall, initial findings suggest that oxytocin and vasopressin systems may mediate early social environment-induced alterations in social behavior. Additional comprehensive studies will be necessary to advance our understanding to what extent changes in oxytocin and vasopressin underlie early social environment-induced alterations in social behavior. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.     

Neural mechanisms of social learning and decision-making

One of the hallmarks of human society is the ubiquitous interactions among individuals. Indeed, a significant portion of human daily routine decision making is socially related. Normative economic theory, namely game theory, has prescribed the canonical decision strategy when "rational" social agents have full information about the decision environment. In reality, however, social decision is often influenced by the trait and state parameters of selves and others. Therefore, understanding the cognitive and neural processes of inferring the decision parameters is pivotal for social decision making. Recently, both correlational and causal non-invasive neuroimaging studies have started to reveal the critical neural computations underlying social learning and decision-making, and highlighted the unique roles of "social" brain structures such as temporal-parietal junction(TPJ) and dorsomedial prefrontal cortex(dmPFC). Here we review recent advances in social decision neuroscience and maintain the focus on how the inference about others is dynamically acquired during social learning, as well as how the prosocial(altruistic)behavior results from orchestrated interactions of different brain regions specified under the social utility framework. We conclude by emphasizing the importance of combining computational decision theory with the identification of neural mechanisms that represent, evaluate and integrate value related social information and generate decision variables guiding behavioral output in the complex social environment.     

Dynamic changes in social dominance and mPOA GnRH expression in male mice following social opportunity

Social competence - the ability of animals to dynamically adjust their social behavior dependent on the current social context – is fundamental to the successful establishment and maintenance of social relationships in group-living species. The social opportunity paradigm, where animals rapidly ascend a social hierarchy following the removal of more dominant individuals, is a well-established approach for studying the neural and neuroendocrine mechanisms underlying socially competent behavior. In the current study, we demonstrate that this paradigm can be successfully adapted for studying socially competent behavior in laboratory mice. Replicating our previous reports, we show that male laboratory mice housed in a semi-natural environment form stable linear social hierarchies. Novel to the current study, we find that subdominant male mice immediately respond to the removal of the alpha male from a hierarchy by initiating a dramatic increase in aggressive behavior towards more subordinate individuals. Consequently, subdominants assume the role of the alpha male. Analysis of brain gene expression in individuals 1 h following social ascent indicates elevated gonadotropin-releasing hormone (GnRH) mRNA levels in the medial preoptic area (mPOA) of the hypothalamus compared to individuals that do not experience a social opportunity. Moreover, hormonal analyses indicate that subdominant individuals have increased circulating plasma testosterone levels compared to subordinate individuals. Our findings demonstrate that male mice are able to dynamically and rapidly adjust both behavior and neuroendocrine function in response to changes in social context. Further, we establish the social opportunity paradigm as an ethologically relevant approach for studying social competence and behavioral plasticity in mammals.     

Neuronal ensemble dynamics in social memory

A large body of evidence suggests that cognitive functions rely on the coordination of ensembles of neurons across brain circuits. One example is social memory, the ability to recognize and remember other conspecifics. A broad range of brain regions have been implicated in social behaviors and memory processes. At the single-cell level, neurons from different brain areas have responded to specific social features. The coordination of these ensembles both within a region and across structures is required to support social memory and decision-making. The synchronous activation of these neuronal ensembles could allow for the integration of different aspects of a social episode into a unified representation of experience. In this review, recent results on the circuit basis and physiological mechanisms of social memory are discussed, from a systems neuroscience perspective. An integrative framework of the neuronal ensemble dynamics supporting this fundamental cognitive ability is proposed.     

Support for the reproductive ground plan hypothesis of social evolution and major QTL for ovary traits of Africanized worker honey bees (Apis mellifera L.)

Background  

The reproductive ground plan hypothesis of social evolution suggests that reproductive controls of a solitary ancestor have been co-opted during social evolution, facilitating the division of labor among social insect workers. Despite substantial empirical support, the generality of this hypothesis is not universally accepted. Thus, we investigated the prediction of particular genes with pleiotropic effects on ovarian traits and social behavior in worker honey bees as a stringent test of the reproductive ground plan hypothesis. We complemented these tests with a comprehensive genome scan for additional quantitative trait loci (QTL) to gain a better understanding of the genetic architecture of the ovary size of honey bee workers, a morphological trait that is significant for understanding social insect caste evolution and general insect biology.     

前额叶皮层在社交行为中的作用

社交行为对于个体身心健康和社会发展都极其重要。社交行为障碍已成为多种精神类疾病的典型临床表征,对个体的发展有严重不良影响。前额叶皮层作为调节社交行为的关键脑区之一,参与了社交、情绪、决策等高级功能,其内部神经元、神经胶质细胞的活动变化及相互作用对调节社交行为有着重要影响,而且前额叶皮层与其他脑区之间的协作也会影响不同的社会行为。本文回顾了前额叶皮层中神经元、神经胶质细胞以及脑区投射与社交行为关系的最新研究,系统综述了前额叶皮层在社交行为调节中的作用,以期为社交障碍的神经机制和有效诊疗提供参考。     

Octopamine neuromodulatory effects on a social behavior decision-making network in Drosophila males

Situations requiring rapid decision-making in response to dynamic environmental demands occur repeatedly in natural environments. Neuromodulation can offer important flexibility to the output of neural networks in coping with changing conditions, but the contribution of individual neuromodulatory neurons in social behavior networks remains relatively unknown. Here we manipulate the Drosophila octopaminergic system and assay changes in adult male decision-making in courtship and aggression paradigms. When the functional state of OA neural circuits is enhanced, males exhibit elevated courtship behavior towards other males in both behavioral contexts. Eliminating the expression of the male form of the neural sex determination factor, Fruitless (Fru(M)), in three OA suboesophageal ganglia (SOG) neurons also leads to increased male-male courtship behavior in these same contexts. We analyzed the fine anatomical structure through confocal examination of labeled single neurons to determine the arborization patterns of each of the three Fru(M)-positive OA SOG neurons. These neurons send processes that display mirror symmetric, widely distributed arbors of endings within brain regions including the ventrolateral protocerebra, the SOG and the peri-esophageal complex. The results suggest that a small subset of OA neurons have the potential to provide male selective modulation of behavior at a single neuron level.     

Progesterone impairs social recognition in male rats

The influence of progesterone in the brain and on the behavior of females is fairly well understood. However, less is known about the effect of progesterone in the male system. In male rats, receptors for progesterone are present in virtually all vasopressin (AVP) immunoreactive cells in the bed nucleus of the stria terminalis (BST) and the medial amygdala (MeA). This colocalization functions to regulate AVP expression, as progesterone and/or progestin receptors (PR)s suppress AVP expression in these same extrahypothalamic regions in the brain. These data suggest that progesterone may influence AVP-dependent behavior. While AVP is implicated in numerous behavioral and physiological functions in rodents, AVP appears essential for social recognition of conspecifics. Therefore, we examined the effects of progesterone on social recognition. We report that progesterone plays an important role in modulating social recognition in the male brain, as progesterone treatment leads to a significant impairment of social recognition in male rats. Moreover, progesterone appears to act on PRs to impair social recognition, as progesterone impairment of social recognition is blocked by a PR antagonist, RU-486. Social recognition is also impaired by a specific progestin agonist, R5020. Interestingly, we show that progesterone does not interfere with either general memory or olfactory processes, suggesting that progesterone seems critically important to social recognition memory. These data provide strong evidence that physiological levels of progesterone can have an important impact on social behavior in male rats.     

Minocycline modulates human social decision-making: possible impact of microglia on personality-oriented social behaviors

Background

Microglia, one of the glial cells, play important roles in various brain pathologies including psychiatric disorders. In addition, microglia have recently been proved to monitor synaptic reactions via direct-touching even in normal brain. Human microglia may modulate various social/mental functions, while microglial social/mental roles remain unresolved especially in healthy humans. There is no known drug with the specific effect of modulating microglia. Therefore, using minocycline, a tetracycline antibiotic and the most famous microglial inhibitor, is one of the best alternative approaches to clarify microglial functions on human social/mental activities.

Methodology/Principal Findings

We conducted a double-blind randomized trial of trust game, a monetary decision-making experiment, with ninety-nine human adult males who decided how much to trust an anonymous partner after a four-day administration of minocycline. Our previous pilot trial indicated a positive effect of minocycline, while the underlying mechanisms were not clarified. Therefore, in this trial with larger samples, we additionally measured the effects of anxiety and personality. The monetary score in trust game was significantly lower in the minocycline group. Interestingly, participants’ ways of decision-making were significantly shifted; cooperativeness, one component of personality, proved to be the main modulating factor of decision-making in the placebo group, on the other hand, the minocycline group was mainly modulated by state anxiety and trustworthiness.

Conclusions/Significance

Our results suggest that minocycline led to more situation-oriented decision-making, possibly by suppressing the effects of personality traits, and furthermore that personality and social behaviors might be modulated by microglia. Early-life events may activate human microglia, establish a certain neuro-synaptic connection, and this formation may determine each human’s personality and personality- oriented social behaviors in later life. To explore these mechanisms, further translational research is needed.

Trial Registration

UMIN clinical trial center UMIN000004803     

An acute social defeat stressor in early puberty increases susceptibility to social defeat in adulthood

Syrian hamsters readily display territorial aggression. If they lose even a single agonistic encounter, however, hamsters show striking reductions in aggressive behavior and increases in submissive behavior, a distinct behavioral change that we have previously termed conditioned defeat. This acute social defeat stressor is primarily psychological and is effective in both males and females. Therefore, we maintain that this procedure presents an ideal model for studying behavioral and physiological responses to social stress. Here, we demonstrate that social avoidance following social defeat is a particularly useful dependent measure because of its sensitivity and stability between sexes and across the estrous cycle. In addition, we demonstrate that peripubertal hamsters exposed to a single, 15 min social defeat exhibit significantly more social avoidance 24 h later when compared with no-defeat controls. Later, defeated and non-defeated hamsters display similar agonistic behavior in adulthood indicating that the peripubertal defeat does not alter adult territorial aggression. After experiencing an additional social defeat in adulthood, however, the hamsters that experienced the pubertal defeat respond to the adult defeat with increased social avoidance when compared with hamsters that were defeated only in adulthood and with no-defeat controls. These data are the first to show that a single social defeat in puberty increases susceptibility to later social defeat in both males and females.     

Neurological correlates of social behavior

Experimental evidence obtained over the past decade in nonhuman primates suggests that there are neural structures necessary for the maintenance of social bonds and affiliative behavior. These include the amygdaloid nuclei, which is the critical brain area, and two anatomically closely related cortical structures—the temporal pole and posterior medial orbital cortex. Bilateral ablation of any of the areas results in a syndrome that varies from a quantitative decrease in affiliative behavior in confined colonies to total social isolation in naturally free-ranging groups. Lesions of these areas in adult females are also incompatible with the maintenance of the maternal-infant bond, but operated infants thrive and are well cared for. Species-typical behavior will determine the response of group members to lesioned conspecifics, and may vary from attempts to reintegrate the affected subject to attack and ostracism.The amygdaloid nuclei are hypothesized to be essential to placing an emotional bias on sensory information; thus this brain area is sensitive to, and its function dependent on, the social/environmental context of ongoing behavior. Brain impairment per se, does not necessarily result in ostracism and may be compatible with maintenance of social bondings depending upon the neural structures involved, subject's affective state, communication ability, and species typical behaviors. Observations of brain-impaired humans closely parallel studies in nonhuman primates.     

Spécificité des dilemmes éthiques résultant des travaux développés en neurosciences: émergence d’une neuroéthique

As neurosciences improve our knowledge about the brain for defining behaviour, medical ethics and social policy, what are the implications of new possibilities of technical intervention on our brain? Neuroethics defines a new field of ethics where scientists and ethicists, and also journalists and politicians, are beginning to reflect on social issues resulting from applications of the work of neuroscience in areas such as moral vision, decision-making, conduct and policies. It is likely that the potential application of new knowledge to human behaviour will generate a great deal of ethical and public policy concern in many aspects of everyday life, from child care and school programs to improvements or maintenance of adult capabilities. Neuroscience will also challenge social fields as diverse as forensic psychiatry, sports, corporate hiring and the judiciary. As neurosciences advance, it is important to have a framework that might help to guide the utilization of the new knowledge.     

The vasopressin 1b receptor and the neural regulation of social behavior

To date, much of the work in rodents implicating vasopressin (Avp) in the regulation of social behavior has focused on its action via the Avp 1a receptor (Avpr1a). However, there is mounting evidence that the Avp 1b receptor (Avpr1b) also plays a significant role in Avp's modulation of social behavior. The Avpr1b is heavily expressed on the anterior pituitary cortiocotrophs where it acts as an important modulator of the endocrine stress response. In the brain, the Avpr1b is prominent in the CA2 region of the hippocampus, but can also be found in areas such as the paraventricular nucleus of the hypothalamus and the olfactory bulb. Studies that have employed genetic knockouts or pharmacological manipulation of the Avpr1b point to the importance of central Avpr1b in the modulation of social behavior. However, there continues to be a knowledge gap in our understanding of where in the brain this is occurring, as well as how and if the central actions of Avp acting via the Avpr1b interact with the stress axis. In this review we focus on the genetic and pharmacological studies that have implicated the Avpr1b in the neural regulation of social behaviors, including social forms of aggressive behavior, social memory, and social motivation. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.     

The regulation of social recognition, social communication and aggression: vasopressin in the social behavior neural network

Neuropeptides in the arginine vasotocin/arginine vasopressin (AVT/AVP) family play a major role in the regulation of social behavior by their actions in the brain. In mammals, AVP is found within a circuit of recriprocally connected limbic structures that form the social behavior neural network. This review examines the role played by AVP within this network in controlling social processes that are critical for the formation and maintenance of social relationships: social recognition, social communication and aggression. Studies in a number of mammalian species indicate that AVP and AVP V1a receptors are ideally suited to regulate the expression of social processes because of their plasticity in response to factors that influence social behavior. The pattern of AVP innervation and V1a receptors across the social behavior neural network may determine the potential range and intensity of social responses that individuals display in different social situations. Although fundamental information on how social behavior is wired in the brain is still lacking, it is clear that different social behaviors can be influenced by the actions of AVP in the same region of the network and that AVP can act within multiple regions of this network to regulate the expression of individual social behaviors. The existing data suggest that AVP can influence social behavior by modulating the interpretation of sensory information, by influencing decision making and by triggering complex motor outputs. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.     

Behavior as a social construction

Behavior analysis is examined from a social constructionist perspective. Constructionism is first defined and contrasted with a generic positivistic image of science. Behavior analysis, especially the matching law, is then viewed from both perspectives. The actual practice of behavior analysis (as opposed to the philosophy of radical behaviorism) more strongly resembles positivist than constructionist views. This alignment between behavior analysis and positivism emerges more sharply when positivist and constructionist perspectives are compared on the relation between science and music. Charles Rosen has identified how the classical style of musical composition and performance depended on 18th century keyboard technology, and a constructionist view sees the matching law as reflecting mid 20th century technology and culture in much the same way as it sees, say Mozart's 23rd piano concerto, as reflecting late 18th century culture. Behavior analysts, who often behave as though they see the matching law as an objective, impersonal, stable, hard, cold, incontrovertibly true fact, appear more inclined than constructionists to see a fundamental difference between the matching law and Mozart's 23rd piano concerto, to which they would attribute few if any of these characteristics. Possible implications are derived for tolerance in science.     

Coevolutionary relationship between striatum size and social play in nonhuman primates

The striatum is a region of the brain specifically tied to the experience and anticipation of pleasure, reward, appropriate behavioral sequencing, cognition, learning, and social modulation. Furthermore, the striatum is connected neurologically and functionally to other brain regions associated with the exhibition of social play, such as the neocortex, cerebellum, and limbic system. For these reasons, the striatum is especially interesting to researchers of play behavior. Moreover, the caudate-putamen area of the striatum has been specifically implicated in laboratory studies of social play behavior. This study uses the phylogenetic comparative method of independent contrasts to test for an evolutionary relationship between striatum volume and a measure of social play in nonhuman primates. Relative volume of the primate striatum correlates with rate of social, but not nonsocial, play behavior across species, suggesting a coevolution of traits. The pleasurable and procedural aspects of social play behavior may be mediated in part by the striatum and further to its connection to dopaminergic pathways in the primate brain.     

Neuropeptidergic regulation of affiliative behavior and social bonding in animals

Social relationships are essential for maintaining human mental health, yet little is known about the brain mechanisms involved in the development and maintenance of social bonds. Animal models are powerful tools for investigating the neurobiological mechanisms regulating the cognitive processes leading to the development of social relationships and for potentially extending our understanding of the human condition. In this review, we discuss the roles of the neuropeptides oxytocin and vasopressin in the regulation of social bonding as well as related social behaviors which culminate in the formation of social relationships in animal models. The formation of social bonds is a hierarchical process involving social motivation and approach, the processing of social stimuli and formation of social memories, and the social attachment itself. Oxytocin and vasopressin have been implicated in each of these processes. Specifically, these peptides facilitate social affiliation and parental nurturing behavior, are essential for social recognition in rodents, and are involved in the formation of selective mother-infant bonds in sheep and pair bonds in monogamous voles. The convergence of evidence from these animal studies makes oxytocin and vasopressin attractive candidates for the neural modulation of human social relationships as well as potential therapeutic targets for the treatment of psychiatric disorders associated with disruptions in social behavior, including autism.     

Evidence for social role in a dolphin social network

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