Neural and Molecular Mechanisms of Biological Embedding of Social Interactions.

Animals operate in complex environments, and salient social information is encoded in the nervous system and then processed to initiate adaptive behavior. This encoding involves biological embedding, the process by which social experience affects the brain to influence future behavior. Biological embedding is an important conceptual framework for understanding social decision-making in the brain, as it encompasses multiple levels of organization that regulate how information is encoded and used to modify behavior. The framework we emphasize here is that social stimuli provoke short-term changes in neural activity that lead to changes in gene expression on longer timescales. This process, simplified-neurons are for today and genes are for tomorrow-enables the assessment of the valence of a social interaction, an appropriate and rapid response, and subsequent modification of neural circuitry to change future behavioral inclinations in anticipation of environmental changes. We review recent research on the neural and molecular basis of biological embedding in the context of social interactions, with a special focus on the honeybee.

An Aggressive Interaction Rapidly Increases Brain Androgens in a Male Songbird during the Non-breeding Season.

Aggression is a crucial behavior that impacts access to limited resources in different environmental contexts. Androgens synthesized by the gonads promote aggression during the breeding season. However, aggression can be expressed during the non-breeding season, despite low androgen synthesis by the gonads. The brain can also synthesize steroids ("neurosteroids"), including androgens, which might promote aggression during the non-breeding season. Male song sparrows, Melospiza melodia, are territorial year-round and allow the study of seasonal changes in the steroid modulation of aggression. Here, we quantified steroids following a simulated territorial intrusion (STI) for 10 min in wild adult male song sparrows during the breeding and non-breeding seasons. Using liquid chromatography-tandem mass spectrometry (LC-MS/MS), we examined 11 steroids: pregnenolone, progesterone, corticosterone, dehydroepiandrosterone, androstenedione, testosterone, 5α-dihydrotestosterone, 17ß-estradiol, 17α-estradiol, estriol, and estrone. Steroids were measured in blood and 10 microdissected brain regions that regulate social behavior. In both seasons, STI increased corticosterone in the blood and brain. In the breeding season, STI had no rapid effects on androgens or estrogens. Intriguingly, in the non-breeding season, STI increased testosterone and androstenedione in several behaviorally relevant regions, but not in the blood, where androgens remained non-detectable. Also in the non-breeding season, STI increased progesterone in the blood and specific brain regions. Overall, rapid socially modulated changes in brain steroid levels are more prominent during the non-breeding season. Brain steroid levels vary with season and social context in a region-specific manner and suggest a role for neuroandrogens in aggression during the non-breeding season.

The Neuroscience of Human and Artificial Intelligence Presence.

Two decades of social neuroscience and neuroeconomics research illustrate the brain mechanisms that are engaged when people consider human beings, often in comparison to considering artificial intelligence (AI) as a nonhuman control. AI as an experimental control preserves agency and facilitates social interactions but lacks a human presence, providing insight into brain mechanisms that are engaged by human presence and the presence of AI. Here, I review this literature to determine how the brain instantiates human and AI presence across social perception and decision-making paradigms commonly used to realize a social context. People behave toward humans differently than they do toward AI. Moreover, brain regions more engaged by humans compared to AI extend beyond the social cognition brain network to all parts of the brain, and the brain sometimes is engaged more by AI than by humans. Finally, I discuss gaps in the literature, limitations in current neuroscience approaches, and how an understanding of the brain correlates of human and AI presence can inform social science in the wild.

Breakdown of utilitarian moral judgement after basolateral amygdala damage.

Most of us would regard killing another person as morally wrong, but when the death of one saves multiple others, it can be morally permitted. According to a prominent computational dual-systems framework, in these life-and-death dilemmas, deontological (nonsacrificial) moral judgments stem from a model-free algorithm that emphasizes the intrinsic value of the sacrificial action, while utilitarian (sacrificial) moral judgments are derived from a model-based algorithm that emphasizes the outcome of the sacrificial action. Rodent decision-making research suggests that the model-based algorithm depends on the basolateral amygdala (BLA), but these findings have not yet been translated to human moral decision-making. Here, in five humans with selective, bilateral BLA damage, we show a breakdown of utilitarian sacrificial moral judgments, pointing at deficient model-based moral decision-making. Across an established set of moral dilemmas, healthy controls frequently sacrifice one person to save numerous others, but BLA-damaged humans withhold such sacrificial judgments even at the cost of thousands of lives. Our translational research confirms a neurocomputational hypothesis drawn from rodent decision-making research by indicating that the model-based algorithm which underlies outcome-based, utilitarian moral judgements in humans critically depends on the BLA.

The effect of acute social isolation on neural molecular responses in components of the social decision-making network.

Prolonged or chronic social isolation has pronounced effects on animals, ranging from altered stress responses, increased anxiety and aggressive behaviour, and even increased mortality. The effects of shorter periods of isolation are much less well researched; however, short periods of isolation are used routinely for testing animal behaviour and physiology. Here, we studied how a 3 h period of isolation from a cagemate affected neural gene expression in three brain regions that contain important components of the social decision-making network, the hypothalamus, the nucleus taeniae of the amygdala, and the bed nucleus of the stria terminalis, using a gregarious bird as a model (zebra finches). We found evidence suggestive of altered neural activity, synaptic transmission, metabolism, and even potentially pain perception, all of which could create cofounding effects on experimental tests that involve isolating animals. We recommend that the effects of short-term social isolation need to be better understood and propose alternatives to isolating animals for testing.

Are older adults less generous? Age differences in emotion-related social decision making.

In social interaction, age-related differences in emotional processing may lead to varied social decision making between young and older adults. However, previous studies of social decision making have paid less attention to the interactants' emotions, leaving age differences and underlying neural mechanisms unexplored. To address this gap, the present study combined functional and structural magnetic resonance imaging, employing a modified dictator game task with recipients displaying either neutral or sad facial expressions. Behavioral results indicated that although older adults' overall allocations did not differ significantly from those of young adults, older adults' allocations showing a decrease in emotion-related generosity compared to young adults. Using representational similarity analysis, we found that older adults showed reduced neural representations of recipients' emotions and gray matter volume in the right anterior cingulate gyrus (ACC), right insula, and left dorsomedial prefrontal cortex (DMPFC) compared to young adults. More importantly, mediation analyses indicated that age influenced allocations not only through serial mediation of neural representations of the right insula and left DMPFC, but also through serial mediation of the mean gray matter volume of the right ACC and left DMPFC. This study identifies the potential neural pathways through which age affects emotion-related social decision making, advancing our understanding of older adults' social interaction behavior that they may not be less generous unless confronted with individuals with specific emotions.

Neural correlates of static and dynamic social decision-making in real-time sibling interactions.

In traditional game theory tasks, social decision-making is centered on the prediction of the intentions (i.e., mentalizing) of strangers or manipulated responses. In contrast, real-life scenarios often involve familiar individuals in dynamic environments. Further research is needed to explore neural correlates of social decision-making with changes in the available information and environmental settings. This study collected fMRI hyperscanning data (N = 100, 46 same-sex pairs were analyzed) to investigate sibling pairs engaging in an iterated Chicken Game task within a competitive context, including two decision-making phases. In the static phase, participants chose between turning (cooperate) and continuing (defect) in a fixed time window. Participants could estimate the probability of different events based on their priors (previous outcomes and representation of other's intentions) and report their decision plan. The dynamic phase mirrored real-world interactions in which information is continuously changing (replicated within a virtual environment). Individuals had to simultaneously update their beliefs, monitor the actions of the other, and adjust their decisions. Our findings revealed substantial choice consistency between the two phases and evidence for shared neural correlates in mentalizing-related brain regions, including the prefrontal cortex, temporoparietal junction (TPJ), and precuneus. Specific neural correlates were associated with each phase; increased activation of areas associated with action planning and outcome evaluation were found in the static compared with the dynamic phase. Using the opposite contrast, dynamic decision-making showed higher activation in regions related to predicting and monitoring other's actions, including the anterior cingulate cortex and insula. Cooperation (turning), compared with defection (continuing), showed increased activation in mentalizing-related regions only in the static phase, while defection, relative to cooperation, exhibited higher activation in areas associated with conflict monitoring and risk processing in the dynamic phase. Men were less cooperative and had greater TPJ activation. Sibling competitive relationship did not predict competitive behavior but showed a tendency to predict brain activity during dynamic decision-making. Only individual brain activation results are included here, and no interbrain analyses are reported. These neural correlates emphasize the significance of considering varying levels of information available and environmental settings when delving into the intricacies of mentalizing during social decision-making among familiar individuals.

The involvement of rTPJ in intention attribution during social decision making: A TMS study.

The mini-Ultimatum Game (mini-UG) is a bargaining game used to assess the reactions of a responder to unfair offers made by a proposer under different intentionality conditions. Previous studies employing this task showed the activation of responders' right temporoparietal junction (rTPJ), which could be related to its involvement in judgments of intentionality. To verify this hypothesis, in the present study we applied online transcranial magnetic stimulation (TMS) over the rTPJ in responders during the mini-UG, in which we manipulated intention attribution implicitly. A cover story was employed to induce participants to believe they were interacting with another agent. We expected that interfering with the rTPJ could affect the ability of responders to assume proposers' perspective, producing higher rates of rejections of unfair offers when offers are perceived as independent from responders' intentionality to inequality. Twenty-six healthy women voluntarily participated in the study. In the mini-UG, an unfair distribution of the proposer (8/2 offer) was pitted against one of three alternative offers: fair-alternative (5/5), no-alternative (8/2), hyperfair-alternative (2/8). During the task, a train of TMS pulses was delivered at proposers' offer presentation in blocks of active (rTPJ) or control (Vertex) stimulation according to an ABAB design. As expected, findings showed that rejection of the no-alternative offers was higher under TMS stimulation of the rTPJ compared with the control TMS. This effect was modulated by the degree of trustworthiness in the cover story. These data contribute defining the mechanisms and brain areas underpinning social decision making as assessed by bargaining tasks.

Value-based neural representations predict social decision preferences.

Social decision-making is omnipresent in everyday life, carrying the potential for both positive and negative consequences for the decision-maker and those closest to them. While evidence suggests that decision-makers use value-based heuristics to guide choice behavior, very little is known about how decision-makers' representations of other agents influence social choice behavior. We used multivariate pattern expression analyses on fMRI data to understand how value-based processes shape neural representations of those affected by one's social decisions and whether value-based encoding is associated with social decision preferences. We found that stronger value-based encoding of a given close other (e.g. parent) relative to a second close other (e.g. friend) was associated with a greater propensity to favor the former during subsequent social decision-making. These results are the first to our knowledge to explicitly show that value-based processes affect decision behavior via representations of close others.

Memory as a foundation for approach and avoidance decisions: A fertile area for research.

Scant research has directly measured the extent episodic memory serves as the basis for decisions, particularly decisions to approach or avoid other people (i.e., social targets). In this theoretical paper, we survey the limited work showing the relationship between episodic memory and subsequent approach or avoidance decisions about social targets, including descriptions of significant limitations of past work. We then describe three important areas for future work in this domain (explicit memory, implicit memory, diagnosticity) as a framework to generate new foundational knowledge about the extent memory influences approach and avoidance decisions. Overall, the framework proposed in this work should lead to better understanding of the connection between memory and decision-making, especially decisions to approach or avoid social targets (i.e., other people).

A role of anterior cingulate cortex in the emergence of worker-parasite relationship.

We studied the brain mechanisms underlying action selection in a social dilemma setting in which individuals' effortful gains are unfairly distributed among group members. A stable "worker-parasite" relationship developed when three individually operant-conditioned rats were placed together in a Skinner box equipped with response lever and food dispenser on opposite sides. Specifically, one rat, the "worker," engaged in lever-pressing while the other two "parasitic" rats profited from the worker's effort by crowding the feeder in anticipation of food. Anatomically, c-Fos expression in the anterior cingulate cortex (ACC) was significantly higher in worker rats than in parasite rats. Functionally, ACC inactivation suppressed the worker's lever-press behavior drastically under social, but only mildly under individual, settings. Transcriptionally, GABAA receptor- and potassium channel-related messenger RNA expressions were reliably lower in the worker's, relative to parasite's, ACC. These findings indicate the requirement of ACC activation for the expression of exploitable, effortful behavior, which could be mediated by molecular pathways involving GABAA receptor/potassium channel proteins.

Decision-making regarding social situations in people with intellectual disability at different stages of the decision-making process.

Decision-making capability is essential in fulfilling the need for autonomy of people with intellectual disability. In this study we aimed to examine decision-making capability regarding important social situations in people with intellectual disability at different stages of decision-making process. We studied 80 vocational school students with mild intellectual disability and 80 students of a similar age from mass vocation schools. We assessed decision-making with Important Life Decisions Task (ILDT). Students with intellectual disability obtained significantly lower scores than controls for each of the stories in ILDT as in each stage and overall final score in the decision-making process. The magnitude of difference in scores between groups varied in different stages of decision-making process. The most notable difficulties in decision-making regarding important social situations in people with intellectual disability are related to the evaluation of alternatives stage. Pattern of differences obtained in our study may be related to the content of decision-making problems.

The effect of an embodied intervention on responsibility: put a load on one's shoulder.

Responsibility is an essential part of our social life. Although responsibility is an abstract concept, it can be represented with concrete ideas through conceptual metaphor. Expressions like "carry a lot of responsibility," "shoulder the responsibility" shows that responsibility can be understood as a load on shoulder that one has to carry. Accordingly, this study tests the question that does putting a burden on one's shoulder makes him/her more responsible or not. In order to investigate this, on each trial, we asked participants to decide between risky situations that vary in magnitude, probability of win/lose, and the ambiguity level in two conditions: "self" and 'group." Each subject wears a vest with a load on each shoulder in half of the trials. As expected, Most of participants choose to defer on the group trials more than on the self-trials. This difference between numbers of deferring in group and self conditions is called responsibility aversion. Results indicate that responsibility aversion scores are lower (responsibility-taking was greater) in the state of wearing the vest than in the form of not wearing the vest significantly. We provided evidence that the abstract concept of responsibility is linked to bodily experiences of feeling load on the shoulder consistent with an embodied cognition theory.

Higher subjective socioeconomic status is linked to increased charitable giving and mentalizing-related neural value coding.

Socioeconomic status (SES), a concept related to an individual's economic and social position relative to others, can shape social interactions like altruistic behaviors. However, little is known about the exact neurocognitive mechanisms that link SES with altruism. Our study aimed to provide a comprehensive account of the sociocognitive and neural mechanisms through which SES affects charitable giving - an important variant of human altruism. To this end, participants completed a charitable donation task while their brain activity was measured using functional magnetic resonance imaging (fMRI). We also assessed participants' socio-cognitive ability to infer other people's mental states (i.e., mentalizing) - a driver of prosocial behavior - in an independent social task. Behaviorally, we found that both charitable giving and social cognition were status-dependent, as subjective SES positively predicted donations and mentalizing capacity. Moreover, the link between SES and charitable giving was mediated by individuals' mentalizing capacity. At the neural level, a multivariate pattern analysis of fMRI data revealed that higher subjective SES was associated with stronger value coding in the right temporoparietal junction (rTPJ). The strength of this value representation predicted charitable giving and was linked to mentalizing. Furthermore, we observed an increased negative functional coupling between rTPJ and left putamen with higher SES. Together, increased charitable giving in higher-status individuals could be explained by status-dependent recruitment of mentalizing-related value coding and altered functional connectivity in the brain. Our findings provide insights into the socio- and neurocognitive mechanisms explaining why and when higher SES leads to prosociality, which might ultimately inform targeted interventions to promote prosocial behavior in human societies.

A neural circuit perspective on brain aromatase.

This review explores the role of aromatase in the brain as illuminated by a set of conserved network-level connections identified in several vertebrate taxa. Aromatase-expressing neurons are neurochemically heterogeneous but the brain regions in which they are found are highly-conserved across the vertebrate lineage. During development, aromatase neurons have a prominent role in sexual differentiation of the brain and resultant sex differences in behavior and human brain diseases. Drawing on literature primarily from birds and rodents, we delineate brain regions that express aromatase and that are strongly interconnected, and suggest that, in many species, aromatase expression essentially defines the Social Behavior Network. Moreover, in several cases the inputs to and outputs from this core Social Behavior Network also express aromatase. Recent advances in molecular and genetic tools for neuroscience now enable in-depth and taxonomically diverse studies of the function of aromatase at the neural circuit level.

Altered social decision making in patients with chronic pain.

BACKGROUND: Chronic pain affects up to 20% of the population, impairs quality of life and reduces social participation. Previous research reported that pain-related perceived injustice covaries with these negative consequences. The current study probed whether chronic pain patients responded more strongly to disadvantageous social inequity than healthy individuals. METHODS: We administered the Ultimatum Game, a neuroeconomic social exchange game, where a sum of money is split between two players to a large sample of patients with chronic pain disorder with somatic and psychological factors (n = 102) and healthy controls (n = 101). Anonymised, and in truth experimentally controlled, co-players proposed a split, and our participants either accepted or rejected these offers. RESULTS: Chronic pain patients were hypersensitive to disadvantageous inequity and punished their co-players for proposed unequal splits more often than healthy controls. Furthermore, this systematic shift in social decision making was independent of patients' performance on tests of executive functions and risk-sensitive (non-social) decision making . CONCLUSIONS: Our findings indicate that chronic pain is associated with anomalies in social decision making (compared to healthy controls) and hypersensitivity to social inequity that is likely to negatively impact social partaking and thereby the quality of life.

Varied impacts of social relationships on neuroendocrine state.

Social relationships, affiliative social attachments, are important for many species. The best studied types of relationships are monogamous pair bonds. However, it remains unclear how generalizable models of pair bonding are across types of social attachments. Zebra finches are a fascinating system to explore the neurobiology of social relationships because they form various adult bonds with both same- and opposite-sex partners. To test whether different bonds are supported by a single brain network, we quantified individuals' neuroendocrine state after either 24 h or 2 weeks of co-housing with a novel same- or opposite-sex partner. We defined neuroendocrine state by the expression of 22 genes related to 4 major signaling pathways (dopamine, steroid, nonapeptide, and opioid) in six brain regions associated with affiliation or communication [nucleus accumbens (NAc), nucleus taeniae of the amygdala (TnA), medial preoptic area (POM), and periaqueductal gray (PAG), ventral tegmental area, and auditory cortex]. Overall, we found dissociable effects of social contexts (same- or opposite-sex partnerships) and duration of co-housing. Social bonding impacted the neuroendocrine state of four regions in males (NAc, TnA, POM, and PAG) and three regions in females (NAc, TnA, and POM). Monogamous pair bonding specifically appeared to impact male NAc. However, the patterns of gene expression in zebra finches were different than has previously been reported in mammals. Together, our results support the view that there are numerous mechanisms regulating social relationships and highlight the need to further our understanding of how social interactions shape social bonds.

Chronic intranasal oxytocin increases acoustic eavesdropping and adult neurogenesis.

Social information gathering is a complex process influenced by neuroendocrine-modulated neural plasticity. Oxytocin (OXT) is a key regulator of social decision-making processes such as information gathering, as it contextually modulates social salience and can induce long-term structural plasticity, including neurogenesis. Understanding the link between OXT-induced plasticity and communicative awareness is crucial, particularly because OXT is being considered for treatment of social pathologies. We investigated the role of chronic OXT-dependent plasticity in attention to novel social information by manipulating the duration of time following cessation of intranasal treatment to allow for the functional integration of adult-born neurons resulting from OXT treatment. Following a 3-week delay, chronic intranasal OXT (IN-OXT) increased approach behavior of both female and male mice towards aggressive vocal playbacks of two unseen novel conspecifics, while no effect was observed after a 3-day delay. Immature neurons increased in the ventral hippocampus of females and males treated with chronic IN-OXT after the 3-week delay, indicating a potential association between ventral hippocampal neurogenesis and approach/acoustic eavesdropping. The less the mouse approached, the higher the level of neurogenesis. Contrary to expectations, the correlation between ventral hippocampal neurogenesis and approach behavior was not affected by IN-OXT, suggesting that other plasticity mechanisms underlie the long-term effects of chronic OXT on social approach. Furthermore, we found a negative correlation between ventral hippocampal neurogenesis and freezing behavior. Overall, our results demonstrate that chronic IN-OXT-induced long-term plasticity can influence approach to vocal information and we further reinforced the link between neurogenesis and anxiety.

Impacts of repeated social defeat on behavior and the brain in a cichlid fish.

Social defeat is a powerful experience leading to drastic changes in physiology and behavior, many of which are negative. For example, repeated social defeat in vertebrates results in reduced reproductive success, sickness and behavioral abnormalities that threaten individual survival and species persistence. However, little is known about what neural mechanisms are involved in determining whether an individual is resilient or susceptible to repeated social defeat stress. It also remains unknown whether exclusive use of reactive behaviors after repeated social defeat is maintained over time and impacts future behaviors during subsequent contests. We used a resident-intruder experiment in the African cichlid fish Astatotilapia burtoni to investigate the behavior and neural correlates of these two opposing groups. Behavior was quantified by watching fish during defeat trials and used to distinguish resilient and susceptible individuals. Both resilient and susceptible fish started with searching and freezing behaviors, with searching decreasing and freezing increasing after repeated social defeat. After a 4 day break period, resilient fish used both searching and freezing behaviors during a social defeat encounter with a new resident, while susceptible fish almost exclusively used freezing behaviors. By quantifying neural activation using pS6 in socially relevant brain regions, we identified differential neural activation patterns associated with resilient and susceptible fish and found nuclei that co-varied and may represent functional networks. These data provide the first evidence of specific conserved brain networks underlying social stress resilience and susceptibility in fishes.

Online Assessment of Social Cognition in a Population of Gamers and Gamblers: Results of the eSMILE Study.

The purpose of the eSMILE study was to explore social cognition (SC) in the two behavioural addictions (BAs) included in international classifications: gaming disorder and gambling disorder. In these disorders, cognitive functioning is involved in the development and maintenance of addiction. Nevertheless, SC have received less attention than other cognitive functions. The eSMILE study was conducted online and included 105 participants (gamers and gamblers). This study included: the Penn emotion recognition task, the Condensed and Revised Multifaced Empathy Test, the Interpersonal Reactivity Index, the Chicken Game, social metacognition questions, and the Toronto Alexithymia Scale. We analysed the relationships among SC measures, addiction levels, and behaviour frequency. For gamers, we showed that the higher their level of addiction was, the lower their self-confidence following the identification of basic emotions, although the more frequently they played, the better their performance on this task. Additionally, we found lower performance on the identification of more complex emotions by gamblers, which seems to be the result of their levels of addiction rather than the frequency of their gambling behaviour. This study contributes to our understanding of the cognitive processes underlying BAs. Additionally, working on SC abilities may be an additional management mode for BAs that could be added to existing treatments.