Long-term tracking of social structure in groups of rats.

Rodents serve as an important model for examining both individual and collective behavior. Dominance within rodent social structures can determine access to critical resources, such as food and mating opportunities. Yet, many aspects of the intricate interplay between individual behaviors and the resulting group social hierarchy, especially its evolution over time, remain unexplored. In this study, we utilized an automated tracking system that continuously monitored groups of male rats for over 250 days to enable an in-depth analysis of individual behavior and the overarching group dynamic. We describe the evolution of social structures within a group and additionally investigate how past behaviors influence the emergence of new social hierarchies when group composition and experimental area changes. Notably, we find that conventional individual and pairwise tests exhibit a weak correlation with group behavior, highlighting their limited accuracy in predicting behavioral outcomes in a collective context. These results emphasize the context-dependence of social behavior as an emergent property of interactions within a group and highlight the need to measure and quantify social behavior in more naturalistic environments.

Increased sensitivity to social hierarchy during social competition versus cooperation.

Social hierarchy is a typical feature of social organization. The ability to quickly recognize social hierarchy information is crucial for adapting to social contexts. Here, we adopted fast periodic visual stimulation with electroencephalography to assess the neural responses to social hierarchy during social competition and cooperation, respectively. Participants first learned hierarchical faces from a competitive game versus a cooperative game. We then sequentially presented the learned hierarchical faces with a specific frequency in a set of faces. Results showed that participants rated the inferior player as lower in the social hierarchy in the cooperative context compared to the competitive context, indicating that social context affects the judgment of others' rank. Moreover, higher neural responses to high and low-hierarchy faces versus medium-hierarchy faces were observed, suggesting rapid discrimination of social hierarchy from faces. Interestingly, rank-specific neural responses were more pronounced in the competitive context than in the cooperative context, indicating increased sensitivity to social hierarchy during social competition versus social cooperation. This study provides behavioral and neural evidence for rapid, automatic processing of social hierarchy information and for an increased sensitivity to such information in competitive versus cooperative social contexts.

When social hierarchy matters grammatically: Investigation of the processing of honorifics in Korean.

Korean grammar encodes relative social hierarchies among interlocutors in various ways. This study utilized honorific subject-verb agreement in Korean to investigate how social hierarchies are processed during sentence comprehension. The experimental results showed that honorific violations elicited processing difficulties. The use of an honorific verb with an unhonorifiable subject resulted in lower naturalness ratings, longer reading times, and elicited a P600, similar to effects observed with number, person, and gender agreement in Spanish or English. These findings suggest that social hierarchies have become integrated into grammar, constraining how native Korean speakers process sentences. However, the agreement between honorific subjects and verbs seems asymmetrical; the mismatch effect was smaller or absent when an honorifiable subject was not accompanied by an honorific verb, suggesting that while an honorific verb requires an honorifiable subject, the reverse is not necessarily true. The results indicate that the -si agreement in Korean is a form of morpho-syntactic agreement, despite its asymmetrical nature.

Not All Powerful People Are Created Equal: An Examination of Gender and Pathways to Social Hierarchy Through the Lens of Social Cognition.

Across four studies (N = 816 U.S. adults), we uncovered a gender stereotype about dual pathways to social hierarchy: Men were associated with power, and women were associated with status. We detected this pattern both explicitly and implicitly in perceptions of individuals drawn from Forbes magazine's powerful people lists in undergraduate and online samples. We examined social-cognitive implications, including prominent people's degree of recognition by individuals and society, and the formation of men's and women's self-concepts. We found that power (status) ratings predicted greater recognition of men (women) and lesser recognition of women (men). In terms of the self-concept, we found that women internalized the stereotype associating women with status more than power implicitly and explicitly. Although men explicitly reported having less status and more power than women, men implicitly associated the self with status as much as power. No gender differences emerged in the desires for power and status.

Rank, stress, and risk: A conjecture.

A perception at the core of studies that consider the link between social rank and stress (typically measured by the so-called stress hormone cortisol) is that the link is direct. Examples of such studies are Bartolomucci (2007), Beery and Kaufer (2015), and Koolhaas et al. (2017). A recent and stark representation of this body of work is a study by Smith-Osborne et al. (2023), who state that "social hierarchies directly influence stress status" (Smith-Osborne et al. p. 1537, italics added). In the present paper, we reflect on this "direct" perspective. We conjecture that the link between social rank and stress involves an intervening variable: an indirect relationship arises when the loss of rank triggers a behavioral response in the form of risk taking aimed at regaining rank, and it is the engagement in risk-taking behavior that is the cause of an elevated level of cortisol. Smith-Osborne et al., as well as others whose papers are cited by Smith-Osborne et al. and who, like Creel (2001) and Avitsur et al. (2006), conducted comprehensive research on the association between rank (social standing) and stress, do not refer to risk taking at all. We present four strands of research that lend support to our conjecture: evidence that in response to losing rank, individuals are stressed; evidence that in response to losing rank, individuals resort to risk-taking behavior aimed at regaining their lost rank; evidence that there exists a link between engagement in risky activities or exposure to risk and elevated levels of cortisol; and an analytical perspective on incidence and intensity, namely a perspective that shows how the willingness to take risks responds to a change in rank, specifically, how a loss of rank triggers a greater willingness to take risks and how this trigger is stronger for individuals whose rank is higher.

Social hierarchy differentially influences the anxiety-like behaviors and dendritic spine density in prefrontal cortex and limbic areas in male rats.

Social hierarchy is a fundamental feature of social organization that can influence brain and emotional processing regarding social ranks. Several areas, including the medial prefrontal cortex (mPFC), the hippocampus, and the basolateral nucleus of the amygdala (BLA), are recognized to be involved in the regulation of emotional processing. However, its delicate structural correlates in brain regions are poorly understood. To address this issue, social hierarchy in home-caged sibling Wistar rats (three male rats/cage) was determined by employing a social confrontation tube test (postnatal weeks 9-12). Then, locomotor activity and anxiety-like behaviors were evaluated using an open-field test (OFT) and elevated plus-maze (EPM) at 13 weeks of age. The rapid Golgi impregnation method was conducted to quantify the spine density of the first secondary branch of the primary dendrite in 20 µm length. The results indicated that dominant rats had significantly higher anxiety-like behaviors compared to subordinates, as was evident by lower open-arm entries and time spent in the EPM and lower entries and time spent in the center of OFT. The spine density analysis revealed a significantly higher number of spines in subordinates compared to the dominant rats in dmPFC pyramidal neurons and the apical and basal dendrites of hippocampal CA1 pyramidal neurons. However, the spine density of pyramidal-like neurons in the BLA was higher in dominant rats. Our findings suggest that dominant social rank is associated with higher anxiety and differential density of the dendritic spine in the prefrontal cortex and limbic regions of the brain in male rats.

Transcranial direct current stimulation suggests a causal role of the medial prefrontal cortex in learning social hierarchy.

Social hierarchies can be inferred through observational learning of social relationships between individuals. Yet, little is known about the causal role of specific brain regions in learning hierarchies. Here, using transcranial direct current stimulation, we show a causal role of the medial prefrontal cortex (mPFC) in learning social versus non-social hierarchies. In a Training phase, participants acquired knowledge about social and non-social hierarchies by trial and error. During a Test phase, they were presented with two items from hierarchies that were never encountered together, requiring them to make transitive inferences. Anodal stimulation over mPFC impaired social compared with non-social hierarchy learning, and this modulation was influenced by the relative social rank of the members (higher or lower status). Anodal stimulation also impaired transitive inference making, but only during early blocks before learning was established. Together, these findings demonstrate a causal role of the mPFC in learning social ranks by observation.

Experimentally manipulated anger activates implicit cognitions about social hierarchy.

A correlational pilot study (N = 143) and an integrative data analysis of two experiments (total N = 377) provide evidence linking anger to the psychology of social hierarchy. The experiments demonstrate that the experience of anger increases the psychological accessibility of implicit cognitions related to social hierarchy: compared to participants in a control condition, participants in an anger-priming condition completed word stems with significantly more hierarchy-related words. We found little support for sex differences in the effect of anger on implicit hierarchy-related cognition; effects were equivalent across male and female participants. Findings fit with functionalist evolutionary views of anger suggesting that anger may motivate the use of dominance to strive for high social rank in group hierarchies. Implications for downstream behaviour, including aggression and negotiation, are discussed.

Social rank and compassion: How insecure striving, social safeness and fears of compassion mediate the relationship between masculinity, depression and anxiety.

OBJECTIVE: Traditional masculinity norms displayed by men attempt to signal a dominance or 'toughness' to others; however, traditional masculine norms are associated with a range of mental health difficulties, including depression and anxiety. Based on social rank theory, we tested the mediating role of insecure striving, social safeness and fears of compassion on the relationship between masculinity, anxiety and depression. We also examined whether compassionate goals were negatively correlated with masculine norm adherence. DESIGN: We used a cross-sectional survey design recruiting 844 men, aged 18-60 years (M = 34.0, SD = 14.4). RESULTS: Our results replicated previous findings with masculine norms significantly associated with depression and anxiety. Extending on previous work, we found insecure striving, social safeness and fears of compassion fully mediated these relationships for anxiety and partially for depression. This relationship was strongest for the masculinity subtypes of self-reliance and emotional control. Compassionate goals were negatively associated with masculine norm adherence. CONCLUSIONS: Social rank theory offers a helpful explanatory framework to understand the links between traditional masculinity and mental health, highlighting the importance of social safeness and insecure striving for men.

Transcriptional programming of social hierarchy.

In this issue of Neuron, Choi and colleagues1 uncover the direct role of the transcription factor Pou3f1 in regulating dominance hierarchy in mice. Pou3f1 accomplishes this role via its action in specific prefrontal projection neurons that regulate behaviors associated with low social status.

The impact of social hierarchies on neural response to feedback evaluations after advice giving.

Advisors generally evaluate advisee-relevant feedback after advice giving. The response to these feedback-(1) whether the advice is accepted and (2) whether the advice is optimal-usually involves prestige. Prior literature has found that prestige is the basis by which individuals attain a superior status in the social hierarchy. However, whether advisors are motivated to attain a superior status when engaging in advice giving remains uncharacterized. Using event-related potentials, this study investigates how advisors evaluate feedback after giving advice to superior (vs. inferior) status advisees. A social hierarchy was first established based on two advisees (one was ranked as superior status and another as inferior status) as well as participants' performance in a dot-estimation task in which all participants were ranked as medium status. Participants then engaged in a game in which they were assigned roles as advisors to a superior or inferior status advisee. Afterward, the participants received feedback in two phases. In Phase 1, participants were told whether the advisees accepted the advice provided. In Phase 2, the participants were informed whether the advice they provided was correct. In these two phases, when the advisee was of superior status, participants exhibited stronger feedback-related negativity and P300 difference in response to (1) whether their advice was accepted, and (2) whether their advice was correct. Moreover, the P300 was notably larger when the participants' correct advice led to a gain for a superior-status advisee. In the context of advice giving, advisors are particularly motivated to attain a superior status when the feedback involving social hierarchies, which is reflected in higher sensitivity to feedback associated with superior status advisees at earlier and later stages during feedback evaluations in brains.

Anthropogenic noise limits resource distribution without changing social hierarchies.

Increasing evidence demonstrates that anthropogenic noise is a global pollutant that threatens marine ecosystems. Mounting numbers of studies show its diverse effects on individuals and their behaviour. However, little is known about how individual changes in response to anthropogenic noise could cascade through groups and populations affecting resource distribution vital for survival and fitness. Here we test the hypotheses that anthropogenic noise could alter resource distribution, associated hierarchies and consequently individual benefits. We used groups of hermit crabs, a globally distributed model system for assessing impacts of environmental change on wildlife and measured in controlled laboratory conditions the resource distribution of their reusable shelters (gastropod shells) under ship noise and ambient control playbacks. We applied vacancy chain theory to test three predictions about how new resource units create benefits for a population. A new resource unit leads to (i) a cascade of resource abandonments and acquisitions (= chain of vacancy moves) based on an internal (ii) hierarchy (here size-based) which allows (iii) more than one individual to benefit. All three predictions were supported under control sound. Under anthropogenic noise however, fewer individuals benefitted from the arrival of a new, empty shell, while the size-based hierarchy was maintained. The latter was apparent in chain structures, which were concordant between sound treatments. This experiment shows that anthropogenic noise can affect individual behaviours that cascade through groups. This has the potential to disrupt wider resource distribution in populations.

Inferior social hierarchy is vulnerable to anxiety-like behavior in chronic pain mice: Potential role of gut microbiota and metabolites.

Social dominance is a universal phenomenon among grouped animals that profoundly affects survival, health, and reproductive success by determining access to resources, and exerting a powerful influence on subsequent behavior. However, the understanding of pain and anxiety comorbidities in dominant or subordinate animals suffering from chronic pain is not well-defined. Here, we provide evidence that subordinate mice are more susceptible to pain-induced anxiety compared to dominant mice. We propose that the gut microbiota may play a mediating role in this mechanism. Our findings demonstrate that transplantation of fecal microbiota from subordinate mice with chronic inflammatory pain, but not dominant mice, into antibiotics-treated pseudo-germ-free mice significantly amplifies anxiety-like phenotypes, highlighting the critical involvement of gut microbiota in this behavioral response. Using chronic inflammatory pain model, we carried out 16S rRNA sequencing and untargeted metabolomic analyses to explore the relationship between microbiota and metabolites in a stable social hierarchy of mice. Interestingly, anxiety-like behaviors were directly associated with some microbial genera and metabolites, especially bile acid metabolism. Overall, we have demonstrated a close relationship between social status and anxiety susceptibility, highlighting the contributions of gut microbiota and the associated metabolites in the high-anxiety state of subordinate mice with chronic inflammatory pain.

Dopamine Neuron Activity and Stress Signaling as Links Between Social Hierarchy and Psychopathology Vulnerability.

BACKGROUND: Social status in humans, generally reflected by socioeconomic status, has been associated, when constrained, with heightened vulnerability to pathologies including psychiatric diseases. Social hierarchy in mice translates into individual and interdependent behavioral strategies of animals within a group. The rules leading to the emergence of a social organization are elusive, and detangling the contribution of social status from other factors, whether environmental or genetic, to normal and pathological behaviors remains challenging. METHODS: We investigated the mechanisms shaping the emergence of a social hierarchy in isogenic C57BL/6 mice raised in groups of 4 using conditional mutant mouse models and chemogenetic manipulation of dopamine midbrain neuronal activity. We further studied the evolution of behavioral traits and the vulnerability to psychopathological-like phenotypes according to the social status of the animals. RESULTS: Higher sociability predetermined higher social hierarchy in the colony. Upon hierarchy establishment, higher-ranked mice showed increased anxiety and better cognitive abilities in a working memory task. Strikingly, the higher-ranked mice displayed a reduced activity of dopaminergic neurons within the ventral tegmental area, paired with a decreased behavioral response to cocaine and a decreased vulnerability to depressive-like behaviors following repeated social defeats. The pharmacogenetic inhibition of this neuronal population and the genetic inactivation of glucocorticoid receptor signaling in dopamine-sensing brain areas that resulted in decreased dopaminergic activity promoted accession to higher social ranks. CONCLUSIONS: Dopamine activity and its modulation by the stress response shapes social organization in mice, potentially linking interindividual and social status differences in vulnerability to psychopathologies.

Characterization of social hierarchy formation and maintenance in same-sex, group-housed male and female C57BL/6 J mice.

Social hierarchies are a prevalent feature of all animal groups, and an individual's rank within the group can significantly affect their overall health, typically at the greatest expense of the lowest-ranked individuals, or omegas. These subjects have been shown to exhibit various stress-related phenotypes, such as increased hypothalamic-pituitary axis activity and increased amygdalar corticotropin-releasing factor levels compared to higher-ranked subjects. However, these findings have been primarily characterized in males and in models requiring exhibition of severe aggression. The goals of the current study, therefore, were to characterize the formation and maintenance of social hierarchies using the tube test and palatable liquid competition in same-sex groups of male and female C57BL/6 J mice. We also aimed to examine the effects of tube test-determined social rank on plasma and hypothalamic oxytocin and vasopressin levels, peptides with established roles in social behaviors and the stress response. Lastly, we assessed the effects of environmental enrichment and length of testing on the measures outlined above. Overall, we demonstrated that males and females develop social hierarchies and that these hierarchies can be determined using the tube test. While we were unable to establish a consistent connection between peptide levels and social rank, we observed transient changes in these peptides reflecting complex interactions between social rank, sex, environment, and length of testing. We also found that many male and female omegas began to exhibit passive coping behavior after repeated tube test losses, demonstrating the potential of this assay to serve as a model of chronic, mild psychosocial stress.

The role of legitimizing the social hierarchy in the impact of status on perceived assertiveness and competence.

The present research aimed to examine how perceivers' system-justifying beliefs moderate the way they evaluate high- versus low-status targets on assertiveness and competence. In three experimental studies, we manipulated a target's hierarchical position within his company's organization. Participants rated the target on traits reflecting assertiveness and competence. Their system-justifying beliefs were assessed in an ostensibly unrelated study. Results consistently showed that participants inferred assertiveness from the target's hierarchical position regardless of system justification, whereas the relationship between social status and competence was consistently moderated by system-justifying beliefs: only participants high in system justification ascribed more competence to the high-status target than to the low-status target. These findings are in line with the hypothesis suggesting that inferring competence from high-status positions could rely on the tendency to justify social inequalities, whereas inferring assertiveness would not.

Self- and Other-Orientation in High Rank: A Cultural Psychological Approach to Social Hierarchy.

PUBLIC ABSTRACT: Social hierarchy is one fundamental aspect of human life, structuring interactions in families, teams, and entire societies. In this review, we put forward a new theory about how social hierarchy is shaped by the wider societal contexts (i.e., cultures). Comparing East Asian and Western cultural contexts, we show how culture comprises societal beliefs about who can raise to high rank (e.g., become a leader), shapes interactions between high- and low-ranking individuals (e.g., in a team), and influences human thought and behavior in social hierarchies. Overall, we find cultural similarities, in that high-ranking individuals are agentic and self-oriented in both cultural contexts. But we also find important cross-cultural differences. In East Asian cultural contexts, high-ranking individuals are also other oriented; they are also concerned about the people around them and their relationships. We close with a call to action, suggesting studying social hierarchies in more diverse cultural contexts.

Acetylcholine muscarinic M1 receptors in the rodent prefrontal cortex modulate cognitive abilities to establish social hierarchy.

In most social species, the attainment of social dominance is strongly affected by personality traits. Dominant individuals show better cognitive abilities, however, whether an individual's cognition can determine its social status has remained inconclusive. We found that mice show better cognitive abilities tend to possess a higher social rank after cohousing. The dynamic release of acetylcholine (ACh) in the prelimbic cortex (PL) is correlated with mouse dominance behavior. ACh enhanced the excitability of the PL neurons via acetylcholine muscarinic M1 receptors (M1). Inhibition of M1 impaired mice cognitive performance and induced losing in social competition. Mice with M1 deficiency in the PL performed worse on cognitive behavioral tests, and exhibited lower status when re-grouped with others. Elevating ACh level in the PL of subordinate mice induced winning. These results provide direct evidence for the involvement of M1 in social hierarchy and suggest that social rank can be tuned by altering cognition through cholinergic system.

Himpathy and status: Attitudes to social hierarchy predict reactions to sexual harassment.

In three studies, we tested whether hierarchical preferences could explain differences in punishment recommendations for sexual harassment. Building on research that suggests punishment is used to regulate social hierarchies, we argue that individuals who are motivated to maintain existing hierarchies will treat male perpetrators of sexual harassment with greater leniency, especially when judging perpetrators of high social status. Conversely, we predict that egalitarians-who are motivated to reduce group-based hierarchies-will judge male perpetrators more harshly, especially those of high social status. Given competing theories in the existing literature, we make no predictions about how perpetrator status will affect punishment recommendations overall. Supporting our hypotheses, we found that individuals high on gender system justification and social dominance orientation recommended more lenient punishments to perpetrators. Moreover, an integrative data analysis uncovered an interaction between social dominance orientation and perpetrator status. This interaction was primarily driven by egalitarians, who provided more lenient punishment recommendations to low status perpetrators when compared to high status perpetrators. Contrary to our predictions, we did not find strong evidence that individuals high on social dominance orientation provided harsher judgements to low status perpetrators. Nor did we find strong evidence for a main effect of perpetrator status on punishment recommendations. Taken together, these findings suggest that people punish sexual harassment to bolster or attenuate power structures. This is particularly true of egalitarians, whose emphasis on social equality leads them to judge high status perpetrators of sexual harassment with particular severity.

Neural tracking of social hierarchies in adolescents' real-world social networks.

In the current study, we combined sociometric nominations and neuroimaging techniques to examine adolescents' neural tracking of peers from their real-world social network that varied in social preferences and popularity. Adolescent participants from an entire school district (N = 873) completed peer sociometric nominations of their grade at school, and a subset of participants (N = 117, Mage = 13.59 years) completed a neuroimaging task in which they viewed peer faces from their social networks. We revealed two neural processes by which adolescents track social preference: (1) the fusiform face area, an important region for early visual perception and social categorization, simultaneously represented both peers high in social preference and low in social preference; (2) the dorsolateral prefrontal cortex (DLPFC), which was differentially engaged in tracking peers high and low in social preference. No regions specifically tracked peers high in popularity and only the inferior parietal lobe, temporoparietal junction, midcingulate cortex and insula were involved in tracking unpopular peers. This is the first study to examine the neural circuits that support adolescents' perception of peer-based social networks. These findings identify the neural processes that allow youths to spontaneously keep track of peers' social value within their social network.