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.

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.

The dorsomedial prefrontal cortex prioritizes social learning during rest.

Sociality is a defining feature of the human experience: We rely on others to ensure survival and cooperate in complex social networks to thrive. Are there brain mechanisms that help ensure we quickly learn about our social world to optimally navigate it? We tested whether portions of the brain's default network engage "by default" to quickly prioritize social learning during the memory consolidation process. To test this possibility, participants underwent functional MRI (fMRI) while viewing scenes from the documentary film, Samsara. This film shows footage of real people and places from around the world. We normed the footage to select scenes that differed along the dimension of sociality, while matched on valence, arousal, interestingness, and familiarity. During fMRI, participants watched the "social" and "nonsocial" scenes, completed a rest scan, and a surprise recognition memory test. Participants showed superior social (vs. nonsocial) memory performance, and the social memory advantage was associated with neural pattern reinstatement during rest in the dorsomedial prefrontal cortex (DMPFC), a key node of the default network. Moreover, it was during early rest that DMPFC social pattern reinstatement was greatest and predicted subsequent social memory performance most strongly, consistent with the "prioritization" account. Results simultaneously update 1) theories of memory consolidation, which have not addressed how social information may be prioritized in the learning process, and 2) understanding of default network function, which remains to be fully characterized. More broadly, the results underscore the inherent human drive to understand our vastly social world.

Bumblebees acquire alternative puzzle-box solutions via social learning.

The astonishing behavioural repertoires of social insects have been thought largely innate, but these insects have repeatedly demonstrated remarkable capacities for both individual and social learning. Using the bumblebee Bombus terrestris as a model, we developed a two-option puzzle box task and used open diffusion paradigms to observe the transmission of novel, nonnatural foraging behaviours through populations. Box-opening behaviour spread through colonies seeded with a demonstrator trained to perform 1 of the 2 possible behavioural variants, and the observers acquired the demonstrated variant. This preference persisted among observers even when the alternative technique was discovered. In control diffusion experiments that lacked a demonstrator, some bees spontaneously opened the puzzle boxes but were significantly less proficient than those that learned in the presence of a demonstrator. This suggested that social learning was crucial to proper acquisition of box opening. Additional open diffusion experiments where 2 behavioural variants were initially present in similar proportions ended with a single variant becoming dominant, due to stochastic processes. We discuss whether these results, which replicate those found in primates and birds, might indicate a capacity for culture in bumblebees.

Social learning and memory.

The adaptability of human populations to changing environments is often attributed to the human capacity for social learning, innovation, and culture. In rapidly changing environments, it has been shown that maintaining high levels of cultural variation is beneficial because it allows for efficient adaptation. However, in many theoretical models, a high level of cultural variation also implies that a large amount of useless and perhaps detrimental information must be maintained and used, leading to lower population fitness in general. Here, we begin to investigate this often conflicting relationship between adaptation and cultural variation. We explicitly allow for the interplay between social learning and environmental variability, alongside the capacity for "memory," i.e., the storage, retrieval, and forgetting of information. Here, memory allows individuals to retain unexpressed cultural variation, which does not directly impact adaptation. We show that this capacity for memory facilitates the evolution of social learning across a broader range of circumstances than previously thought. Results from this analysis may help to establish whether and when memory should be incorporated into cultural evolutionary models focused on questions of adaptation.

The neural and computational systems of social learning.

Learning the value of stimuli and actions from others - social learning - adaptively contributes to individual survival and plays a key role in cultural evolution. We review research across species targeting the neural and computational systems of social learning in both the aversive and appetitive domains. Social learning generally follows the same principles as self-experienced value-based learning, including computations of prediction errors and is implemented in brain circuits activated across task domains together with regions processing social information. We integrate neural and computational perspectives of social learning with an understanding of behaviour of varying complexity, from basic threat avoidance to complex social learning strategies and cultural phenomena.

Disentangling genetic, plastic and social learning drivers of sex-specific foraging behaviour in Trinidadian guppies (Poecilia reticulata).

Evolutionary biologists have long been interested in parsing out the roles of genetics, plasticity and their interaction on adaptive trait divergence. Since males and females often have different ecological and reproductive roles, separating how their traits are shaped by interactions between their genes and environment is necessary and important. Here, we disentangle the sex-specific effects of genetic divergence, developmental plasticity, social learning and contextual plasticity on foraging behaviour in Trinidadian guppies (Poecilia reticulata) adapted to high- or low-predation habitats. We reared second-generation siblings from both predation regimes with or without predator chemical cues, and with adult conspecifics from either high- or low-predation habitats. We then quantified their foraging behaviour in water with and without predator chemical cues. We found that high-predation guppies forage more efficiently than low-predation guppies, but this behavioural difference is context-dependent and shaped by different mechanisms in males and females. Higher foraging efficiency in high-predation females is largely genetically determined, and to a smaller extent socially learned from conspecifics. However, in high-predation males, higher foraging efficiency is plastically induced by predator cues during development. Our study demonstrates sex-specific differences in genetic versus plastic responses in foraging behaviour, a trait of significance in organismal fitness and ecosystem dynamics.

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.

Environmental harshness does not affect the propensity for social learning in great tits, Parus major.

According to the harsh environment hypothesis, natural selection should favour cognitive mechanisms to overcome environmental challenges. Tests of this hypothesis to date have largely focused on asocial learning and memory, thus failing to account for the spread of information via social means. Tests in specialized food-hoarding birds have shown strong support for the effects of environmental harshness on both asocial and social learning. Whether the hypothesis applies to non-specialist foraging species remains largely unexplored. We evaluated the relative importance of social learning across a known harshness gradient by testing generalist great tits, Parus major, from high (harsh)- and low (mild)-elevation populations in two social learning tasks. We showed that individuals use social learning to find food in both colour-associative and spatial foraging tasks and that individuals differed consistently in their use of social learning. However, we did not detect a difference in the use or speed of implementing socially observed information across the elevational gradient. Our results do not support predictions of the harsh environment hypothesis suggesting that context-dependent costs and benefits as well as plasticity in the use of social information may play an important role in the use of social learning across environments. Finally, this study adds to the accumulating evidence that the harsh environment hypothesis appears to have more pronounced effects on specialists compared to generalist species.

Auditory risk recognition is socially transmitted across territory borders in wild birds.

Prey species commonly assess predation risk based on acoustic signals, such as predator vocalizations or heterospecific alarm calls. The resulting risk-sensitive decision-making affects not only the behavior and life-history of individual prey, but also has far-reaching ecological consequences for population, community, and ecosystem dynamics. Although auditory risk recognition is ubiquitous in animals, it remains unclear how individuals gain the ability to recognize specific sounds as cues of a threat. Here, it has been shown that free-living birds (Wood Warblers Phylloscopus sibilatrix) can learn to recognize unfamiliar, complex sounds (samples of punk rock songs) as cues of a threat from conspecifics holding adjacent territories during the spring breeding season. In a playback experiment, Wood Warblers initially ignored the unfamiliar sounds, but after repeatedly hearing that these sounds trigger alarm calling reaction of neighbors, most individuals showed an anti-predator response to them. Moreover, once learned soon after nestlings hatching, the anti-predator response of parents toward previously unfamiliar sounds was then retained over the entire nestlings rearing period. These results demonstrate that social learning via the association of unfamiliar sounds with known alarm signals enables the spread of anti-predator behavior across territory borders and provides a mechanism explaining the widespread abilities of animals to assess predation risk based on acoustic cues.

Dynamical system model predicts when social learners impair collective performance.

A key question concerning collective decisions is whether a social system can settle on the best available option when some members learn from others instead of evaluating the options on their own. This question is challenging to study, and previous research has reached mixed conclusions, because collective decision outcomes depend on the insufficiently understood complex system of cognitive strategies, task properties, and social influence processes. This study integrates these complex interactions together in one general yet partially analytically tractable mathematical framework using a dynamical system model. In particular, it investigates how the interplay of the proportion of social learners, the relative merit of options, and the type of conformity response affect collective decision outcomes in a binary choice. The model predicts that, when the proportion of social learners exceeds a critical threshold, a bistable state appears in which the majority can end up favoring either the higher- or lower-merit option, depending on fluctuations and initial conditions. Below this threshold, the high-merit option is chosen by the majority. The critical threshold is determined by the conformity response function and the relative merits of the two options. The study helps reconcile disagreements about the effect of social learners on collective performance and proposes a mathematical framework that can be readily adapted to extensions investigating a wider variety of dynamics.

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.

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.

Patterns and predictors of adolescent engagement in a mindfulness-based social-emotional learning program.

INTRODUCTION: Although mindfulness-based interventions (MBIs) show promise for promoting positive youth development, little is known about student engagement in MBIs. Initial research presents mixed findings in MBI engagement related to participant characteristics, and there is a lack of research examining the influence of context on engagement, despite the critical role context plays in academic engagement. This study examines the contribution of student demographic characteristics and classroom context to MBI engagement. METHODS: Survey engagement data were collected at three time points from 106 ninth grade students (Mage = 14.17 years, 60.4% female, 44.2% Black, 24.8% Hispanic/Latino) who participated in the Be CALM program during the 2021-2022 school year. Latent growth curve modeling was used to examine trajectory of student engagement and assess student and classroom predictors of engagement. RESULTS: There was no overall change in the trajectory of student engagement, although variability was observed across classes. Identifying as Hispanic/Latino was associated with lower engagement (ß = -.25, p = .008), although this did not appear to be related to program experience. Peer connections predicted engagement at the end of the program (ß = .39, p < .001). Post hoc analyses suggested that student engagement may be related to teacher program delivery quality. CONCLUSIONS: Student engagement in MBIs appears related to classroom context more than student characteristics, although further research with larger samples is needed to assess the link between engagement and program outcomes. Findings have implications for designing school-based MBIs and training school staff to deliver them in culturally responsive ways.

Older infants' social learning behavior under uncertainty is modulated by the interaction of face and speech processing.

The origin of face or language influences infants' perceptual processing and social learning behavior. However, it remains unclear how infants' social learning behavior is affected when both information are provided simultaneously. Hence, the current study investigated whether and how infants' social learning in terms of gaze following is influenced by face race and language origin of an interaction partner in an uncertain situation. Our sample consisted of 91 Caucasian infants from German speaking families. They were divided into 2 age groups: Younger infants were 5- to 8-month-old (n = 46) and the older infants 11- to 20-month-old (n = 45). We used a modified online version of the gaze following paradigm by Xiao and colleagues by varying face race (Caucasian, and Asian faces) and language (German and French) of a female actor. We recorded infants looking behavior via webcam and coded it offline. Our results revealed that older but not younger infants were biased to follow the gaze of own-race adults speaking their native language. Our findings show that older infants are clearly influenced by adults' ethnicity and language in social learning situations of uncertainty.

Co-producing knowledge on the use of urban natural space: Participatory system dynamics modelling to understand a complex urban system.

Decision-makers are increasingly asked to act differently in how they respond to complex urban challenges, recognising the value in bringing together and integrating cross-disciplinary, cross-sectoral knowledge to generate effective solutions. Participatory modelling allows to bring stakeholders together, enhance knowledge and understanding of a system, and identify the impacts of interventions to a given problem. This paper uses an interdisciplinary and systems approach to investigate a complex urban problem, using a participatory System Dynamics modelling process as an approach to facilitate learning and co-produce knowledge on the factors influencing the use of urban natural space. Stakeholders used a Systems Dynamics model and interface, as a tool to collectively identify pathways for improving the use of space and simulating their impacts. Under the lens of knowledge co-production, the paper reflects how such mechanisms can lead to the co-production of knowledge and social learning. The findings also contribute to identify ways of increasing the value of urban natural space focusing on urban areas undergoing physical and social transformation, such as the Thamesmead case study, London, UK.

Effective Components of Social Emotional Learning Programs: A Meta-analysis.

Previous reviews have synthesized the impacts of universal school-based social emotional learning (SEL) programs. However, they have yet to attempt a meta-analytic approach with rigorous inclusion criteria to identify the key SEL components and explore what make these programs work. This study aims to fill that gap by examining the impacts of SEL programs and exploring the moderating effects of methodological characteristics, implementation features, and program components on SEL effectiveness. The final sample consisted of 12 high-quality SEL programs, 59 studies, and 83,233 participants, with an overall effect size of 0.15. Meta-regression results indicated that these SEL programs could significantly improve youth social emotional skills, reinforce affect and attitudes, promote academic performance, increase prosocial behaviors, and reduce antisocial behaviors. Training teachers' social emotional skills and reducing cognitive elements in SEL curricula were found to be effective components of SEL programs, whereas pedagogical activities, climate support, and family engagement were not. Large-scale studies of SEL programs tended to generate smaller effect sizes, and those with low program dosages were found to be less effective than those approaching the recommended dosage. Policy and practical implications on how to scale SEL programs are discussed.

Social Learning of Innovations in Dynamic Predator-Prey Systems.

AbstractWe investigate the social transmission of innovations between predators. We focus on two classic predator-prey models. We assume that innovations increase predator attack rates or conversion efficiencies or that innovations reduce predator mortality or handling time. We find that a common outcome is the destabilization of the system. Destabilizing effects include increasing oscillations or limit cycles. Particularly, in more realistic systems (where prey are self-limiting and predators have a type II functional response), destabilization occurs because of overexploitation of the prey. Whenever instability increases the risk of extinction, innovations that benefit individual predators may not have positive long-term effects on predator populations. Additionally, instability could maintain behavioral variability among predators. Interestingly, when predator populations are low despite coexisting with prey populations near their carrying capacity, innovations that could help predators better exploit their prey are least likely to spread. Precisely how unlikely this is depends on whether naive individuals need to observe an informed individual interact with prey to learn the innovation. Our findings help illuminate how innovations could affect biological invasions, urban colonization, and the maintenance of behavioral polymorphisms.

Cultural transmission of move choice in chess.

The study of cultural evolution benefits from detailed analysis of cultural transmission in specific human domains. Chess provides a platform for understanding the transmission of knowledge due to its active community of players, precise behaviours and long-term records of high-quality data. In this paper, we perform an analysis of chess in the context of cultural evolution, describing multiple cultural factors that affect move choice. We then build a population-level statistical model of move choice in chess, based on the Dirichlet-multinomial likelihood, to analyse cultural transmission over decades of recorded games played by leading players. For moves made in specific positions, we evaluate the relative effects of frequency-dependent bias, success bias and prestige bias on the dynamics of move frequencies. We observe that negative frequency-dependent bias plays a role in the dynamics of certain moves, and that other moves are compatible with transmission under prestige bias or success bias. These apparent biases may reflect recent changes, namely the introduction of computer chess engines and online tournament broadcasts. Our analysis of chess provides insights into broader questions concerning how social learning biases affect cultural evolution.