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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

Dopamine D2 receptor within the intermediate region of the lateral septum modulate social hierarchy in male mice.

The dopamine (DA) system has long been involved in social hierarchies; however, the specific mechanisms have not been elucidated. The lateral septum (LS) is a limbic brain structure that regulates various emotional, motivational, and social behaviors. DA receptors are abundantly expressed in the LS, modulating its functions. In this study, we evaluated the functions of DA receptors within different subregions of the LS in social dominance using a confrontation tube test in male mice. The results showed that mice living in social groups formed linear dominance hierarchies after a few days of cohousing, and the subordinates showed increased anxiety. Fos expressions was elevated in the entire LS after a confrontation tube test in the subordinates. However, DA neurons were more activated in the dominates within the ventral tegmental area and the dorsal raphe nucleus. Quantitative real-time polymerase chain reaction results showed that D2 receptor (D2R) within the intermediate region of the LS (LSi) were elevated in the subordinate. In the following pharmacological studies, we found simultaneous D2R activation in the dominants and D2R inhibition in the subordinates switched the original dominant-subordinate relationship. The aforementioned results suggested that D2R within the LSi plays an important role in social dominance in male mice. These findings improve our understanding of the neural mechanisms underlying the social hierarchy, which is closely related to our social life and happiness.

5-HT1A receptor in the central amygdala and 5-HT2A receptor in the basolateral amygdala are involved in social hierarchy in male mice.

Most social animals self-organize into dominance hierarchies that strongly influence their behavior and health. The serotonin (5-HT) system is believed to play an important role in the formation of social hierarchy. 5-HT receptors are abundantly expressed in the amygdala, which is considered as the central node for the perception and learning of social hierarchy. In this study, we assessed the functions of various 5-HT receptor subtypes related to social rank determination in different subregions of the amygdala using the confrontation tube test in mice. We revealed that most adult C57BL/6 J male mice exhibited a linear social rank after a few days of cohousing. The tube test ranks were slightly related to anxiety-like behavioral performance. After the tube test, the amygdala and 5-HT neurons in the dorsal raphe nucleus were activated in lower-rank individuals. Quantitative real-time polymerase chain reaction analysis revealed that despite the high expression of 5-HT1A receptor mRNA in the central amygdala (CeA), 5-HT2A receptor mRNA expression was downregulated in the basolateral amygdala (BLA) in higher-rank individuals. The dominant-subordinate relationship between mouse pairs could be switched via pharmacological modulation of these receptors in CeA and BLA, suggesting that these expression changes are essential for establishing social ranks. Our findings provide novel insights into the divergent functions of 5-HT receptors in the amygdala related to social hierarchy, which is closely related to our health and welfare.

Distinctive Roles of Medial Prefrontal Cortex Subregions in Strategic Conformity to Social Hierarchy.

People often align their behaviors and decisions with others' expectations, especially those of higher social positions, when they are being observed. However, little attention has been paid to the neural mechanisms underlying increased conformity to the social hierarchy under social observation. Using a preference rating task, we investigated whether and how individual preferences for novel stimuli were influenced by others' preferences by manipulating others' social hierarchy and observational context. The behavioral results showed that human participants of both sexes were more likely to change their preferences to match those of a superior partner in a public than in a private context. fMRI data revealed distinct contributions of the subregions of the medial prefrontal cortex (mPFC) to increased conformity to social hierarchy under observation. Specifically, the ventral mPFC showed increased activity when participants' preferences aligned with those of superior partners, regardless of behavioral manifestation. The rostral mPFC showed increased activity when conforming to a superior partner and nonconforming to an inferior one, indicating goal-dependent valuation. The dorsal mPFC showed increased activity in private conditions with a superior partner but only in those with a higher tendency to conform. These findings support the hierarchical allostatic regulation model of the mPFC function for social valuation and suggest strategic conformity as a way to minimize metabolic costs.SIGNIFICANCE STATEMENT This study revealed distinct roles of subregions of the mPFC in increased conformity to individuals of different social ranks under observation. Specifically, the ventral mPFC showed increased activity when participants' preferences aligned with those of higher-ranking partners, whereas the rostral mPFC showed increased activity when conforming to a superior partner and nonconforming to an inferior partner, indicating goal-dependent valuation. The dorsal mPFC was more active in private conditions with a superior partner but only in those with a higher tendency to conform. These findings support the hierarchical allostatic regulation model of the mPFC function for social valuation and suggest strategic conformity as a way to minimize metabolic costs.

Quantifying agonistic interactions between group-housed animals to derive social hierarchies using computer vision: a case study with commercially group-housed rabbits.

In recent years, computer vision has contributed significantly to the study of farm animal behavior. In complex environments such as commercial farms, however, the automated detection of social behavior and specific interactions between animals can be improved. The present study addresses the automated detection of agonistic interactions between caged animals in a complex environment, relying solely on computer vision. An automated pipeline including group-level temporal action segmentation, object detection, object tracking and rule-based action classification for the detection of agonistic interactions was developed and extensively validated at a level unique in the field. Comparing with observations made by human observers, our pipeline reaches 77% precision and 85% recall using a 5-min tolerance interval for the detection of agonistic interactions. Results obtained using this pipeline allow to construct time-dependent socio-matrices of a group of animals and derive metrics on the dominance hierarchy in a semi-automated manner. Group-housed breeding rabbits (does) with their litters in commercial farms are the main use-case in this work, but the idea is probably also applicable to other social farm animals.

Prenatal SAMe Treatment Changes via Epigenetic Mechanism/s USVs in Young Mice and Hippocampal Monoamines Turnover at Adulthood in a Mouse Model of Social Hierarchy and Depression.

The role of hippocampal monoamines and their related genes in the etiology and pathogenesis of depression-like behavior, particularly in impaired sociability traits and the meaning of changes in USVs emitted by pups, remains unknown. We assessed the effects of prenatal administration of S-adenosyl-methionine (SAMe) in Sub mice that exhibit depressive-like behavior on serotonergic, dopaminergic and noradrenergic metabolism and the activity of related genes in the hippocampus (HPC) in adulthood in comparison to saline-treated control Sub mice. During postnatal days 4 and 8, we recorded and analyzed the stress-induced USVs emitted by the pups and tried to understand how the changes in the USVs' calls may be related to the changes in the monoamines and the activity of related genes. The recordings of the USVs showed that SAMe induced a reduction in the emitted flat and one-frequency step-up call numbers in PND4 pups, whereas step-down type calls were significantly increased by SAMe in PND8 pups. The reduction in the number of calls induced by SAMe following separation from the mothers implies a reduction in anxiety, which is an additional sign of decreased depressive-like behavior. Prenatal SAMe increased the concentrations of serotonin in the HPC in both male and female mice without any change in the levels of 5HIAA. It also decreased the level of the dopamine metabolite DOPAC in females. There were no changes in the levels of norepinephrine and metabolites. Several changes in the expression of genes associated with monoamine metabolism were also induced by prenatal SAMe. The molecular and biochemical data obtained from the HPC studies are generally in accordance with our previously obtained data from the prefrontal cortex of similarly treated Sub mice on postnatal day 90. The changes in both monoamines and their gene expression observed 2-3 months after SAMe treatment are associated with the previously recorded behavioral improvement and seem to demonstrate that SAMe is effective via an epigenetic mechanism.