Protocol to study dam-pup social transmission using a modified paradigm for transmission of food preference.

The social transmission of food preference, a rudimentary form of social learning, has primarily been studied in pairs of adult rodents. Here, we present a protocol to explore the parent-offspring context in social learning using an adaptation of this classic paradigm for rodent dam-pup dyads. We describe steps for studying weanling mice from the same mother and present a worked example using weight-based (food consumption) and time-based (exploration) indices of social learning.

Cheerful tails: Delving into positive emotional contagion.

This review delves into the phenomenon of positive emotional contagion (PEC) in rodents, an area that remains relatively understudied compared to the well-explored realm of negative emotions such as fear or pain. Rodents exhibit clear preferences for individuals expressing positive emotions over neutral counterparts, underscoring the importance of detecting and responding to positive emotional signals from others. We thoroughly examine the adaptive function of PEC, highlighting its pivotal role in social learning and environmental adaptation. The developmental aspect of the ability to interpret positive emotions is explored, intricately linked to maternal care and social interactions, with oxytocin playing a central role in these processes. We discuss the potential involvement of the reward system and draw attention to persisting gaps in our understanding of the neural mechanisms governing PEC. Presenting a comprehensive overview of the existing literature, we focus on food-related protocols such as the Social Transmission of Food Preferences paradigm and tickling behaviour. Our review emphasizes the pressing need for further research to address lingering questions and advance our comprehension of positive emotional contagion.

The effect of observing trained conspecifics on the performance and motivation of goldfish, Carassius auratus, in a spatial task.

Spatial and social cognition are two aspects of fish behaviour that have been subject to an increasing amount of research in recent years, but few have investigated potential behaviour overlaps. Testing the ability for an individual to socially learn a spatial task would bridge this gap in understanding. We provided naïve goldfish, Carassius auratus, the opportunity to observe a trained conspecific navigate a T-shaped maze, and then recorded how many trials it took for them to learn the maze, time taken per trial, motivation, and acceptance of the food reward. We also recorded how many trials it took a control group to learn the maze without the opportunity to observe a demonstrator. The observer group took significantly longer to learn the maze than the control group. Although the observer group were significantly less motivated (trials without a choice made), they were significantly more likely to accept the food reward. The social learning of reward acceptance was taking place, but the process of the demonstration disrupted the training of the spatial task, with possible explanations as the passenger effect and trade-off mechanism being discussed. Future studies are needed to determine whether goldfish can acquire spatial information socially; however, this study contributes to the feasibility of studying social learning of environmentally information in goldfish.

A distinct cortical code for socially learned threat.

Animals can learn about sources of danger while minimizing their own risk by observing how others respond to threats. However, the distinct neural mechanisms by which threats are learned through social observation (known as observational fear learning1-4 (OFL)) to generate behavioural responses specific to such threats remain poorly understood. The dorsomedial prefrontal cortex (dmPFC) performs several key functions that may underlie OFL, including processing of social information and disambiguation of threat cues5-11. Here we show that dmPFC is recruited and required for OFL in mice. Using cellular-resolution microendoscopic calcium imaging, we demonstrate that dmPFC neurons code for observational fear and do so in a manner that is distinct from direct experience. We find that dmPFC neuronal activity predicts upcoming switches between freezing and moving state elicited by threat. By combining neuronal circuit mapping, calcium imaging, electrophysiological recordings and optogenetics, we show that dmPFC projections to the midbrain periaqueductal grey (PAG) constrain observer freezing, and that amygdalar and hippocampal inputs to dmPFC opposingly modulate observer freezing. Together our findings reveal that dmPFC neurons compute a distinct code for observational fear and coordinate long-range neural circuits to select behavioural responses.

Visuo-frontal interactions during social learning in freely moving macaques.

Social interactions represent a ubiquitous aspect of our everyday life that we acquire by interpreting and responding to visual cues from conspecifics1. However, despite the general acceptance of this view, how visual information is used to guide the decision to cooperate is unknown. Here, we wirelessly recorded the spiking activity of populations of neurons in the visual and prefrontal cortex in conjunction with wireless recordings of oculomotor events while freely moving macaques engaged in social cooperation. As animals learned to cooperate, visual and executive areas refined the representation of social variables, such as the conspecific or reward, by distributing socially relevant information among neurons in each area. Decoding population activity showed that viewing social cues influences the decision to cooperate. Learning social events increased coordinated spiking between visual and prefrontal cortical neurons, which was associated with improved accuracy of neural populations to encode social cues and the decision to cooperate. These results indicate that the visual-frontal cortical network prioritizes relevant sensory information to facilitate learning social interactions while freely moving macaques interact in a naturalistic environment.

Simplifying social learning.

Social learning is complex, but people often seem to navigate social environments with ease. This ability creates a puzzle for traditional accounts of reinforcement learning (RL) that assume people negotiate a tradeoff between easy-but-simple behavior (model-free learning) and complex-but-difficult behavior (e.g., model-based learning). We offer a theoretical framework for resolving this puzzle: although social environments are complex, people have social expertise that helps them behave flexibly with low cognitive cost. Specifically, by using familiar concepts instead of focusing on novel details, people can turn hard learning problems into simpler ones. This ability highlights social learning as a prototype for studying cognitive simplicity in the face of environmental complexity and identifies a role for conceptual knowledge in everyday reward learning.

A dedicated hypothalamic oxytocin circuit controls aversive social learning.

To survive in a complex social group, one needs to know who to approach and, more importantly, who to avoid. In mice, a single defeat causes the losing mouse to stay away from the winner for weeks1. Here through a series of functional manipulation and recording experiments, we identify oxytocin neurons in the retrochiasmatic supraoptic nucleus (SOROXT) and oxytocin-receptor-expressing cells in the anterior subdivision of the ventromedial hypothalamus, ventrolateral part (aVMHvlOXTR) as a key circuit motif for defeat-induced social avoidance. Before defeat, aVMHvlOXTR cells minimally respond to aggressor cues. During defeat, aVMHvlOXTR cells are highly activated and, with the help of an exclusive oxytocin supply from the SOR, potentiate their responses to aggressor cues. After defeat, strong aggressor-induced aVMHvlOXTR cell activation drives the animal to avoid the aggressor and minimizes future defeat. Our study uncovers a neural process that supports rapid social learning caused by defeat and highlights the importance of the brain oxytocin system in social plasticity.

Expanding the understanding of majority-bias in children's social learning.

Prior experiments with children across seven different societies have indicated U-shaped age patterns in the likelihood of copying majority demonstrations. It is unclear which learning strategies underlie the observed responses that create these patterns. Here we broaden the understanding of children's learning strategies by: (1) exploring social learning patterns among 6-13-year-olds (n = 270) from ethnolinguistically varied communities in Vanuatu; (2) comparing these data with those reported from other societies (n = 629), and (3) re-analysing our and previous data based on a theoretically plausible set of underlying strategies using Bayesian methods. We find higher rates of social learning in children from Vanuatu, a country with high linguistic and cultural diversity. Furthermore, our results provide statistical evidence for modest U-shaped age patterns for a more clearly delineated majority learning strategy across the current and previously investigated societies, suggesting that the developmental mechanisms structuring majority bias are cross-culturally highly recurrent and hence a fundamental feature of early human social learning.

Social behavior mediates the use of social and personal information in wild jays.

The factors favoring the evolution of certain cognitive abilities in animals remain unclear. Social learning is a cognitive ability that reduces the cost of acquiring personal information and forms the foundation for cultural behavior. Theory predicts the evolutionary pressures to evolve social learning should be greater in more social species. However, research testing this theory has primarily occurred in captivity, where artificial environments can affect performance and yield conflicting results. We compared the use of social and personal information, and the social learning mechanisms used by wild, asocial California scrub-jays and social Mexican jays. We trained demonstrators to solve one door on a multi-door task, then measured the behavior of naïve conspecifics towards the task. If social learning occurs, observations of demonstrators will change the rate that naïve individuals interact with each door. We found both species socially learned, though personal information had a much greater effect on behavior in the asocial species while social information was more important for the social species. Additionally, both species used social information to avoid, rather than copy, conspecifics. Our findings demonstrate that while complex social group structures may be unnecessary for the evolution of social learning, it does affect the use of social versus personal information.

Validity and reliability of resiliency measures trialled for the evaluation of a preventative Resilience-promoting social-emotional curriculum for remote Aboriginal school students.

PURPOSE: We aimed to test the reliability and validity of two brief measures of resilience adopted for the evaluation of a preventative social-emotional curriculum implemented for Aboriginal middle school students from socially disadvantaged remote communities in Australia's Northern Territory. The questionnaires chosen were intended to measure psychological resilience and socio-cultural resilience as complementary dimensions of the capacity to cope in circumstances of significant life stress and risk of self-harm. METHODS: Confirmatory factor analysis (CFA) was conducted to assess construct validity of the 10-item Connor-Davidson Resilience Scale (CD-RISC-10), a measure of psychological resilience, and the 12-item Child and Youth Resilience Measure (CYRM-12), a measure of socio-cultural resilience, with a sample of 520 students. Associations between resilience and psychological distress and emotional and behavioural difficulty were analysed in relation to life stressors to assess criterion validity of the scales. RESULTS: CFA provided support for the validity of the respective constructs. There was good fit for both scales. However, assessment of criterion validity of the scales suggested that the adapted measure of socio-cultural resilience (CYRM-12NT) showed higher reliability and a clearer indication of predictive validity than the measure of psychological resilience (CD-RISC-10). CONCLUSIONS: The CYRM-12NT appears to be a more useful measure of resilience among Aboriginal youth exposed to significant life stress and disadvantage. However, both measures may require further development to enhance their validity and utility among potentially at-risk adolescents in socially, culturally and linguistically diverse remote Aboriginal communities.

Childhood in social learning models with changing environments: Implications for human evolution.

Childhood is a time of learning, both individually and through social interactions. But the vulnerability inherent in childhood represents a fitness cost: individuals do not have progeny during childhood, and childhood is a net drain of familial or group resources. In this study we model childhood in resource acquisition scenarios where social learning through observation competes with learning through innovation across multiple generations in a variety of environments. In general, observing others allows useful knowledge to be gained more efficiently than self-exploration and may result in significantly greater resource acquisition. However, social learning needing a lengthy childhood to develop advanced cognitive ability may offset the net fitness advantage that might otherwise be gained. Through simulations we demonstrate that individuals with a substantial childhood burden acquire more lifetime resources by observing others than do individuals with negligible childhood costs using self-exploration, as long as the environment is fairly stable. This advantage decreases as the environment becomes less predictable, and reverses in rapidly changing environments where knowledge is unreliable. These results suggest that hominid evolution, with vastly growing cognitive abilities and a longer, more vulnerable childhood, may have been facilitated in similarly stable environments. On the other hand, hominid populations may have been particularly vulnerable to environmental instability. We apply this insight to the Out of Africa Homo sapiens migration roughly 50,000 years ago and show consistency with the serial founder model that best fits current archeological and genetic evidence. Our findings are important for models of social learning, especially those that describe the emergence and spread of Homo sapiens.

Trusting the experts: The domain-specificity of prestige-biased social learning.

Prestige-biased social learning (henceforth "prestige-bias") occurs when individuals predominantly choose to learn from a prestigious member of their group, i.e. someone who has gained attention, respect and admiration for their success in some domain. Prestige-bias is proposed as an adaptive social-learning strategy as it provides a short-cut to identifying successful group members, without having to assess each person's success individually. Previous work has documented prestige-bias and verified that it is used adaptively. However, the domain-specificity and generality of prestige-bias has not yet been explicitly addressed experimentally. By domain-specific prestige-bias we mean that individuals choose to learn from a prestigious model only within the domain of expertise in which the model acquired their prestige. By domain-general prestige-bias we mean that individuals choose to learn from prestigious models in general, regardless of the domain in which their prestige was earned. To distinguish between domain specific and domain general prestige we ran an online experiment (n = 397) in which participants could copy each other to score points on a general-knowledge quiz with varying topics (domains). Prestige in our task was an emergent property of participants' copying behaviour. We found participants overwhelmingly preferred domain-specific (same topic) prestige cues to domain-general (across topic) prestige cues. However, when only domain-general or cross-domain (different topic) cues were available, participants overwhelmingly favoured domain-general cues. Finally, when given the choice between cross-domain prestige cues and randomly generated Player IDs, participants favoured cross-domain prestige cues. These results suggest participants were sensitive to the source of prestige, and that they preferred domain-specific cues even though these cues were based on fewer samples (being calculated from one topic) than the domain-general cues (being calculated from all topics). We suggest that the extent to which people employ a domain-specific or domain-general prestige-bias may depend on their experience and understanding of the relationships between domains.

Observation of others' threat reactions recovers memories previously shaped by firsthand experiences.

Information about dangers can spread effectively by observation of others' threat responses. Yet, it is unclear if such observational threat information interacts with associative memories that are shaped by the individual's direct, firsthand experiences. Here, we show in humans and rats that the mere observation of a conspecific's threat reactions reinstates previously learned and extinguished threat responses in the observer. In two experiments, human participants displayed elevated physiological responses to threat-conditioned cues after observational reinstatement in a context-specific manner. The elevation of physiological responses (arousal) was further specific to the context that was observed as dangerous. An analogous experiment in rats provided converging results by demonstrating reinstatement of defensive behavior after observing another rat's threat reactions. Taken together, our findings provide cross-species evidence that observation of others' threat reactions can recover associations previously shaped by direct, firsthand aversive experiences. Our study offers a perspective on how retrieval of threat memories draws from associative mechanisms that might underlie both observations of others' and firsthand experiences.

Dopaminergic signaling supports auditory social learning.

Explicit rewards are commonly used to reinforce a behavior, a form of learning that engages the dopaminergic neuromodulatory system. In contrast, skill acquisition can display dramatic improvements from a social learning experience, even though the observer receives no explicit reward. Here, we test whether a dopaminergic signal contributes to social learning in naïve gerbils that are exposed to, and learn from, a skilled demonstrator performing an auditory discrimination task. Following five exposure sessions, naïve observer gerbils were allowed to practice the auditory task and their performance was assessed across days. We first tested the effect of an explicit food reward in the observer's compartment that was yoked to the demonstrator's performance during exposure sessions. Naïve observer gerbils with the yoked reward learned the discrimination task significantly faster, as compared to unrewarded observers. The effect of this explicit reward was abolished by administration of a D1/D5 dopamine receptor antagonist during the exposure sessions. Similarly, the D1/D5 antagonist reduced the rate of learning in unrewarded observers. To test whether a dopaminergic signal was sufficient to enhance social learning, we administered a D1/D5 receptor agonist during the exposure sessions in which no reward was present and found that the rate of learning occurred significantly faster. Finally, a quantitative analysis of vocalizations during the exposure sessions suggests one behavioral strategy that contributes to social learning. Together, these results are consistent with a dopamine-dependent reward signal during social learning.

Lifetime stability of social traits in bottlenose dolphins.

Behavioral phenotypic traits or "animal personalities" drive critical evolutionary processes such as fitness, disease and information spread. Yet the stability of behavioral traits, essential by definition, has rarely been measured over developmentally significant periods of time, limiting our understanding of how behavioral stability interacts with ontogeny. Based on 32 years of social behavioral data for 179 wild bottlenose dolphins, we show that social traits (associate number, time alone and in large groups) are stable from infancy to late adulthood. Multivariate analysis revealed strong relationships between these stable metrics within individuals, suggesting a complex behavioral syndrome comparable to human extraversion. Maternal effects (particularly vertical social learning) and sex-specific reproductive strategies are likely proximate and ultimate drivers for these patterns. We provide rare empirical evidence to demonstrate the persistence of social behavioral traits over decades in a non-human animal.

Immature wild orangutans acquire relevant ecological knowledge through sex-specific attentional biases during social learning.

As a part of growing up, immature orangutans must acquire vast repertoires of skills and knowledge, a process that takes several years of observational social learning and subsequent practice. Adult female and male orangutans show behavioral differences including sex-specific foraging patterns and male-biased dispersal. We investigated how these differing life trajectories affect social interest and emerging ecological knowledge in immatures. We analyzed 15 years of detailed observational data on social learning, associations, and diet repertoires of 50 immatures (16 females and 34 males), from 2 orangutan populations. Specific to the feeding context, we found sex differences in the development of social interest: Throughout the dependency period, immature females direct most of their social attention at their mothers, whereas immature males show an increasing attentional preference for individuals other than their mothers. When attending to non-mother individuals, males show a significant bias toward immigrant individuals and a trend for a bias toward adult males. In contrast, females preferentially attend to neighboring residents. Accordingly, by the end of the dependency period, immature females show a larger dietary overlap with their mothers than do immature males. These results suggest that immature orangutans show attentional biases through which they learn from individuals with the most relevant ecological knowledge. Diversifying their skills and knowledge likely helps males when they move to a new area. In sum, our findings underline the importance of fine-grained social inputs for the acquisition of ecological knowledge and skills in orangutans and likely in other apes as well.

Synchronous caregiving from birth to adulthood tunes humans' social brain.

Mammalian young are born with immature brain and rely on the mother's body and caregiving behavior for maturation of neurobiological systems that sustain adult sociality. While research in animal models indicated the long-term effects of maternal contact and caregiving on the adult brain, little is known about the effects of maternal-newborn contact and parenting behavior on social brain functioning in human adults. We followed human neonates, including premature infants who initially lacked or received maternal-newborn skin-to-skin contact and full-term controls, from birth to adulthood, repeatedly observing mother-child social synchrony at key developmental nodes. We tested the brain basis of affect-specific empathy in young adulthood and utilized multivariate techniques to distinguish brain regions sensitive to others' distinct emotions from those globally activated by the empathy task. The amygdala, insula, temporal pole (TP), and ventromedial prefrontal cortex (VMPFC) showed high sensitivity to others' distinct emotions. Provision of maternal-newborn contact enhanced social synchrony across development from infancy and up until adulthood. The experience of synchrony, in turn, predicted the brain's sensitivity to emotion-specific empathy in the amygdala and insula, core structures of the social brain. Social synchrony linked with greater empathic understanding in adolescence, which was longitudinally associated with higher neural sensitivity to emotion-specific empathy in TP and VMPFC. Findings demonstrate the centrality of synchronous caregiving, by which infants practice the detection and sharing of others' affective states, for tuning the human social brain, particularly in regions implicated in salience detection, interoception, and mentalization that underpin affect sharing and human attachment.

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.

Social reinforcement learning as a predictor of real-life experiences in individuals with high and low depressive symptomatology.

BACKGROUND: Several studies have reported diminished learning from non-social outcomes in depressed individuals. However, it is not clear how depression impacts learning from social feedback. Notably, mood disorders are commonly associated with deficits in social functioning, which raises the possibility that potential impairments in social learning may negatively affect real-life social experiences in depressed subjects. METHODS: Ninety-two participants with high (HD; N = 40) and low (LD; N = 52) depression scores were recruited. Subjects performed a learning task, during which they received monetary outcomes or social feedback which they were told came from other people. Additionally, participants answered questions about their everyday social experiences. Computational models were fit to the data and model parameters were related to social experience measures. RESULTS: HD subjects reported a reduced quality and quantity of social experiences compared to LD controls, including an increase in the amount of time spent in negative social situations. Moreover, HD participants showed lower learning rates than LD subjects in the social condition of the task. Interestingly, across all participants, reduced social learning rates predicted higher amounts of time spent in negative social situations, even when depression scores were controlled for. CONCLUSION: These findings indicate that deficits in social learning may affect the quality of everyday social experiences. Specifically, the impaired ability to use social feedback to appropriately update future actions, which was observed in HD subjects, may lead to suboptimal interpersonal behavior in real life. This, in turn, may evoke negative feedback from others, thus bringing about more unpleasant social encounters.

Oxytocin-induced facilitation of learning in a probabilistic task is associated with reduced feedback- and error-related negativity potentials.

BACKGROUND: Feedback evaluation of actions and error response detection are critical for optimizing behavioral adaptation. Oxytocin can facilitate learning following social feedback but whether its effects vary as a function of feedback valence remains unclear. AIMS: The present study aimed to investigate whether oxytocin would influence responses to positive and negative feedback differentially or equivalently. METHODS: The present study employed a randomized, double-blind, placebo controlled within-subject design to investigate whether intranasal oxytocin (24 IU) influenced behavioral and evoked electrophysiological potential responses to positive or negative feedback in a probabilistic learning task. RESULTS: Results showed that oxytocin facilitated learning and this effect was maintained in the absence of feedback. Using novel stimulus pairings, we found that oxytocin abolished bias towards learning more from negative feedback under placebo by increasing accuracy for positively reinforced stimuli. Oxytocin also decreased the feedback-related negativity difference (negative minus positive feedback) during learning, further suggesting that it rendered the evaluation of positive and negative feedback more equivalent. Additionally, post-learning oxytocin attenuated error-related negativity amplitudes but increased the late error positivity, suggesting that it may lower conflict detection between actual errors and expected correct responses at an early stage of processing but at a later stage increase error awareness and motivation for avoiding them. CONCLUSIONS: Oxytocin facilitates learning and subsequent performance by rendering the impact of positive relative to negative feedback more equivalent and also by reducing conflict detection and increasing error awareness, which may be beneficial for behavioral adaption.