Considering Organismal Physiology in Laboratory Studies of Rodent Behavior.

Any experiment conducted in a rodent laboratory is done so against the backdrop of each animal's physiological state at the time of the experiment. This physiological state can be the product of multiple factors, both internal (e.g., animal sex, strain, hormone cycles, or circadian rhythms) and external (e.g., housing conditions, social status, and light/dark phases). Each of these factors has the potential to influence experimental outcomes, either independently or via interactions with others, and yet there is little consistency across laboratories in terms of the weight with which they are considered in experimental design. Such discrepancies-both in practice and in reporting-likely contribute to the perception of a reproducibility crisis in the field of behavioral neuroscience. In this review, we discuss how several of these sources of variability can impact outcomes within the realm of common learning and memory paradigms.

Humans flexibly integrate social information despite interindividual differences in reward.

There has been much progress in understanding human social learning, including recent studies integrating social information into the reinforcement learning framework. Yet previous studies often assume identical payoffs between observer and demonstrator, overlooking the diversity of social information in real-world interactions. We address this gap by introducing a socially correlated bandit task that accommodates payoff differences among participants, allowing for the study of social learning under more realistic conditions. Our Social Generalization (SG) model, tested through evolutionary simulations and two online experiments, outperforms existing models by incorporating social information into the generalization process, but treating it as noisier than individual observations. Our findings suggest that human social learning is more flexible than previously believed, with the SG model indicating a potential resource-rational trade-off where social learning partially replaces individual exploration. This research highlights the flexibility of humans' social learning, allowing us to integrate social information from others with different preferences, skills, or goals.

Callousness, exploitativeness, and tracking of cooperation incentives in the human default network.

Human cognitive capacities that enable flexible cooperation may have evolved in parallel with the expansion of frontoparietal cortical networks, particularly the default network. Conversely, human antisocial behavior and trait antagonism are broadly associated with reduced activity, impaired connectivity, and altered structure of the default network. Yet, behaviors like interpersonal manipulation and exploitation may require intact or even superior social cognition. Using a reinforcement learning model of decision-making on a modified trust game, we examined how individuals adjusted their cooperation rate based on a counterpart's cooperation and social reputation. We observed that learning signals in the default network updated the predicted utility of cooperation or defection and scaled with reciprocal cooperation. These signals were weaker in callous (vs. compassionate) individuals but stronger in those who were more exploitative (vs. honest and humble). Further, they accounted for associations between exploitativeness, callousness, and reciprocal cooperation. Separately, behavioral sensitivity to prior reputation was reduced in callous but not exploitative individuals and selectively scaled with responses of the medial temporal subsystem of the default network. Overall, callousness was characterized by blunted behavioral and default network sensitivity to cooperation incentives. Exploitativeness predicted heightened sensitivity to others' cooperation but not social reputation. We speculate that both compassion and exploitativeness may reflect cognitive adaptations to social living, enabled by expansion of the default network in anthropogenesis.

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.

Teachers recruit mentalizing regions to represent learners' beliefs.

Teaching enables humans to impart vast stores of culturally specific knowledge and skills. However, little is known about the neural computations that guide teachers' decisions about what information to communicate. Participants (N = 28) played the role of teachers while being scanned using fMRI; their task was to select examples that would teach learners how to answer abstract multiple-choice questions. Participants' examples were best described by a model that selects evidence that maximizes the learner's belief in the correct answer. Consistent with this idea, participants' predictions about how well learners would do closely tracked the performance of an independent sample of learners (N = 140) who were tested on the examples they had provided. In addition, regions that play specialized roles in processing social information, namely the bilateral temporoparietal junction and middle and dorsal medial prefrontal cortex, tracked learners' posterior belief in the correct answer. Our results shed light on the computational and neural architectures that support our extraordinary abilities as teachers.

Learning through the grapevine and the impact of the breadth and depth of social networks.

We study how communication platforms can improve social learning without censoring or fact-checking messages, when they have members who deliberately and/or inadvertently distort information. Message fidelity depends on social network depth (how many times information can be relayed) and breadth (the number of others with whom a typical user shares information). We characterize how the expected number of true minus false messages depends on breadth and depth of the network and the noise structure. Message fidelity can be improved by capping depth or, if that is not possible, limiting breadth, e.g., by capping the number of people to whom someone can forward a given message. Although caps reduce total communication, they increase the fraction of received messages that have traveled shorter distances and have had less opportunity to be altered, thereby increasing the signal-to-noise ratio.

Independent, but still observant-dog breeds selected for functional independence learn better from a conspecific demonstrator than cooperative breeds in a detour task.

BACKGROUND: While complex dog-human coexistence has been deeply investigated, there is a relative scarcity of similar knowledge regarding dog-dog interactions. Social learning, a fundamental synchronizing mechanism between dogs and humans, was recently found to be influenced by the functional breed selection of dogs: with the cooperative breeds being more effective learners from a human demonstrator than the independent working breeds were. Here, we investigated whether these differences would also be present when dogs had to learn from another dog and how to effectively perform a detour around a transparent V-shaped obstacle. We tested dogs from 28 independent and 19 cooperative breeds in three consecutive trials. In the control groups, all dogs had to detour on their own the obstacle. In the dog demonstration groups, in trial 1, the subjects had to detour on their own, but before the next two trials, a trained dog showed them the solution. RESULTS: We found that the performance of the two breed groups was the same in the without demonstration groups. However, after observing the dog demonstrator, the independent dogs learned the task more successfully than the cooperative breeds did. In the case of the independent working breeds, detour latencies significantly dropped along the consecutive trials, and these dogs also showed higher rate of successful detours after observing the demonstrator dog's action than in the control group. CONCLUSIONS: This is the first study where the consequences of functional breed selection were confirmed in a scenario that involved conspecific social learning in dogs. The results fit well to the ecologically valid framework of the evolutionary past of dog breed formation, in which cooperative breeds were selected for their interactivity with humans, whereas independent breeds often had to work together with their conspecifics.

You talkin' to me? Functional breed selection may have fundamentally influenced dogs' sensitivity to human verbal communicative cues.

BACKGROUND: The ability to learn from humans via observation was considered to be equally present across properly socialized dogs. We showed recently that cooperative working breeds learned from a human demonstrator more effectively. We hypothesized that functional breed selection could affect sensitivity to human attention-eliciting behavior. Accordingly, we ran the first ever study on dogs that compared the effect of ostensive and neutral verbal communication in a social learning scenario. We used the detour paradigm around a transparent V-shaped fence with either ostensive (addressing the receiver both with words and specific, attention-eliciting prosody) or neutral speech (monotonous reciting of a short poem) demonstration. The other features (gestures, movement) of the demonstration sequence were kept identical between the two conditions. We tested (N = 70) companion dogs from 17 cooperative and 16 independent breeds in three 1-min trials. Subjects had to obtain the reward by detouring around the fence. RESULTS: Detour latencies of the cooperative dogs improved after both ostensive and neutral speech demonstrations. The independent dogs did not improve their detour latency in either of the conditions. Remarkably, ostensive verbal utterances elicited longer relative looking time towards the demonstrator, cooperative dogs looked longer at the demonstrator, and longer looking time resulted in more successful detours. CONCLUSIONS: Our study provides the first indication that functional breed selection had a significant impact on dogs' sensitivity to ostensive human communication, which, apart from being crucially important for social learning from humans, until now was considered as a uniformly present heritage of domestication in dogs.

The acquired dyad inclination and decreased interpersonal brain communication in the pursuit of collective benefit.

People perform better collectively than individually, a phenomenon known as the collective benefit. To pursue the benefit, they may learn from previous behaviors, come to know whose initial opinion should be valued, and develop the inclination to take it as the collective one. Such learning may affect interpersonal brain communication. To test these hypotheses, this study recruited participant dyads to conduct a perceptual task on which they made individual decisions first and then the collective one. The enhanced interpersonal brain synchronization (IBS) between participants was explored when individual decisions were in disagreement vs. agreement. Computational modeling revealed that participant dyads developed the dyad inclination of taking the higher-able participants', not the lower-able ones' decisions as their collective ones. Brain analyses unveiled the enhanced IBS at frontopolar areas, premotor areas, supramarginal gyri, and right temporal-parietal junctions. The premotor IBS correlated negatively with dyad inclination and collective benefit in the absence of correction. The Granger causality analyses further supported the negative relation of dyad inclination with inter-brain communication. This study highlights that dyads learn to weigh individuals' decisions, resulting in dyad inclinations, and explores associated inter-brain communication, offering insights into the dynamics of collective decision-making.

Understanding the Role of Naive Learners in Cultural Change.

AbstractA change to a population's social network is a change to the substrate of cultural transmission, affecting behavioral diversity and adaptive cultural evolution. While features of network structure such as population size and density have been well studied, less is understood about the influence of social processes such as population turnover-or the repeated replacement of individuals by naive individuals. Experimental data have led to the hypothesis that naive learners can drive cultural evolution by better assessing the relative value of behaviors, although this hypothesis has been expressed only verbally. We conducted a formal exploration of this hypothesis using a generative model that concurrently simulated its two key ingredients: social transmission and reinforcement learning. We simulated competition between high- and low-reward behaviors while varying turnover magnitude and tempo. Variation in turnover influenced changes in the distributions of cultural behaviors, irrespective of initial knowledge-state conditions. We found optimal turnover regimes that amplified the production of higher reward behaviors through two key mechanisms: repertoire composition and enhanced valuation by agents that knew both behaviors. These effects depended on network and learning parameters. Our model provides formal theoretical support for, and predictions about, the hypothesis that naive learners can shape cultural change through their enhanced sampling ability. By moving from experimental data to theory, we illuminate an underdiscussed generative process that can lead to changes in cultural behavior, arising from an interaction between social dynamics and learning.

Oxygen loss compromises growth and cognition of cuttlefish newborns.

Ocean deoxygenation and standing levels of hypoxia are shrinking fundamental niches, particularly in coastal areas, yet documented repercussions on species development and behaviour are limited. Here, we tackled the impacts of deoxygenation (7 mg O2 l-1), mild hypoxia (nocturnal 5 mg O2 l-1) and severe hypoxia (nocturnal 2 mg O2 l-1) on cuttlefish (Sepia officinalis) development (hatching success, development time, mantle length), cognition (ability to learn individually and socially) and behaviour (ability to camouflage and to explore its surroundings spatially). We found that hypoxia yielded lower survival rates, smaller body sizes and inhibited predatory (increased latency to attack the prey) and anti-predator (camouflage) behaviours. Acute and chronic exposure to low oxygen produced similar effects on cognition (inability to socially learn, increased open-field activity levels, no changes in thigmotaxis). It is thus expected that, although cuttlefish can withstand oxygen limitation to a certain degree, expanding hypoxic zones will diminish current habitat suitability.

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.

Evolution of reciprocity with limited payoff memory.

Direct reciprocity is a mechanism for the evolution of cooperation in repeated social interactions. According to the literature, individuals naturally learn to adopt conditionally cooperative strategies if they have multiple encounters with their partner. Corresponding models have greatly facilitated our understanding of cooperation, yet they often make strong assumptions on how individuals remember and process payoff information. For example, when strategies are updated through social learning, it is commonly assumed that individuals compare their average payoffs. This would require them to compute (or remember) their payoffs against everyone else in the population. To understand how more realistic constraints influence direct reciprocity, we consider the evolution of conditional behaviours when individuals learn based on more recent experiences. Even in the most extreme case that they only take into account their very last interaction, we find that cooperation can still evolve. However, such individuals adopt less generous strategies, and they cooperate less often than in the classical setup with average payoffs. Interestingly, once individuals remember the payoffs of two or three recent interactions, cooperation rates quickly approach the classical limit. These findings contribute to a literature that explores which kind of cognitive capabilities are required for reciprocal cooperation. While our results suggest that some rudimentary form of payoff memory is necessary, it suffices to remember a few interactions.

Mate-choice copying accelerates species range expansion.

Mate-choice copying is a type of social learning in which females can change their mate preference after observing the choice of others. This behaviour can potentially affect population evolution and ecology, namely through increased dispersal and reduced local adaptation. Here, we simulated the effects of mate-choice copying in populations expanding across an environmental gradient to understand whether it can accelerate or retard the expansion process. Two mate-choice copying strategies were used: (i) when females target a single individual and (ii) when females target similar individuals. We also simulated cases where the male trait singled out by females with mate choice maps perfectly onto his genotype or is influenced by genotype-by-environment interactions. These rules have different effects on the results. When a trait is determined by genotype alone, populations where copier females target all similar males expand faster and the number of potential copiers increased. However, when preference is determined by genotype-by-environment interactions, populations where copier females target a single male had higher dispersal and also expand faster, but the potential number of copiers decreases. The results show that mate-choice copying can accelerate the expansion process, although its adaptiveness depends on the information animals use in different contexts.

Misplaced Divides? Discussing Political Disagreement With Strangers Can Be Unexpectedly Positive.

Differences of opinion between people are common in everyday life, but discussing those differences openly in conversation may be unnecessarily rare. We report three experiments (N = 1,264 U.S.-based adults) demonstrating that people's interest in discussing important but potentially divisive topics is guided by their expectations about how positively the conversation will unfold, leaving them more interested in having a conversation with someone who agrees versus disagrees with them. People's expectations about their conversations, however, were systematically miscalibrated such that people underestimated how positive these conversations would be-especially in cases of disagreement. Miscalibrated expectations stemmed from underestimating the degree of common ground that would emerge in conversation and from failing to appreciate the power of social forces in conversation that create social connection. Misunderstanding the outcomes of conversation could lead people to avoid discussing disagreements more often, creating a misplaced barrier to learning, social connection, free inquiry, and free expression.

Cultural transmission, competition for prey, and the evolution of cooperative hunting.

Although cooperative hunting is widespread among animals, its benefits are unclear. At low frequencies, cooperative hunting may allow predators to escape competition and access bigger prey that could not be caught by a lone cooperative predator. Cooperative hunting is a more successful strategy when it is common, but its spread can result in overhunting big prey, which may have a lower per-capita growth rate than small prey. We construct a one-predator species, two-prey species model in which predators either learn to hunt small prey alone or learn to hunt big prey cooperatively. Predators first learn vertically from parents, then horizontally (i.e. socially) from random individuals or siblings. After horizontal transmission, they hunt with their learning partner if both are cooperative, and otherwise they hunt alone. Cooperative hunting cannot evolve when initially rare unless predators (a) interact with siblings, or (b) horizontally transmit the cooperative behavior to potential hunting partners. Whereas competition for small prey favors cooperative hunting when this cooperation is initially rare, the frequency of cooperative hunting cannot reach 100% unless big prey is abundant. Furthermore, a mutant that increases horizontal learning can invade if cooperative hunting is present, but not at 100%, because horizontal learning allows pairs of predators to have the same strategy. Our results reveal that the interactions between prey availability, social learning, and degree of cooperation among predators may have important effects on ecosystems.

Social demonstration of colour preference improves the learning of associated demonstrated actions.

We studied how different types of social demonstration improve house sparrows' (Passer domesticus) success in solving a foraging task that requires both operant learning (opening covers) and discrimination learning (preferring covers of the rewarding colour). We provided learners with either paired demonstration (of both cover opening and colour preference), action-only demonstration (of opening white covers only), or no demonstration (a companion bird eating without covers). We found that sparrows failed to learn the two tasks with no demonstration, and learned them best with a paired demonstration. Interestingly, the action of cover opening was learned faster with paired rather than action-only demonstration despite being equally demonstrated in both. We also found that only with paired demonstration, the speed of operant (action) learning was related to the demonstrator's level of activity. Colour preference (i.e. discrimination learning) was eventually acquired by all sparrows that learned to open covers, even without social demonstration of colour preference. Thus, adding a demonstration of colour preference was actually more important for operant learning, possibly as a result of increasing the similarity between the demonstrated and the learned tasks, thereby increasing the learner's attention to the actions of the demonstrator. Giving more attention to individuals in similar settings may be an adaptive strategy directing social learners to focus on ecologically relevant behaviours and on tasks that are likely to be learned successfully.

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.

Revisiting Perdeck's massive avian migration experiments debunks alternative social interpretations.

Whether avian migrants can adapt to their changing world depends on the relative importance of genetic and environmental variation for the timing and direction of migration. In the classic series of field experiments on avian migration, A. C. Perdeck discovered that translocated juveniles failed to reach goal areas, whereas translocated adults performed 'true-goal navigation'. His translocations of > 14 000 common starlings (Sturnus vulgaris) suggested that genetic mechanisms guide juveniles into a population-specific direction, i.e. 'vector navigation'. However, alternative explanations involving social learning after release in juveniles could not be excluded. By adding historical data from translocation sites, data that was unavailable in Perdeck's days, and by integrated analyses including the original data, we could not explain juvenile migrations from possible social information upon release. Despite their highly social behaviour, our findings are consistent with the idea that juvenile starlings follow inherited information and independently reach their winter quarters. Similar to more solitarily migrating songbirds, starlings would require genetic change to adjust the migration route in response to global change.

A dyadic investigation of shy children's behavioral and affective responses to delivering a speech.

Shyness is typically associated with avoidant social behavior and restricted affect in new social situations. However, we know considerably less about how one child's shyness influences another child's behavior and affect in new social situations. Children's shyness was parent-reported when children were age 3 (N = 105, 52 girls, Mage = 3.50 years), and children were tested approximately 1 year later (Mage = 4.76 years) in same-gender dyads where they were asked to give an impromptu speech about their most recent birthday in front of an experimenter and the other member of the dyad. We examined whether children's shyness and speech order influenced their own and their social partner's observed behavior and affect during the speech. Regardless of speech order, children's own shyness was positively associated with their own avoidant social behavior and gaze aversion. Regardless of shyness, children who gave their speech second averted their gaze more than children who gave their speech first. We also found that children who gave their speech second displayed less positive affect if their social partner who they watched give the speech first was shyer. We speculate that some 4-year-old children may be sensitive to the avoidant behaviors of their shy peers and, in turn, respond with less animation when it is their turn to participate in the same activity. RESEARCH HIGHLIGHTS: We examined whether preschool children's shyness and speech order influenced their own and their social partner's observed behavior and affect during a dyadic speech task Children's own shyness was positively associated with their own avoidant social behavior and gaze aversion Children who gave their speech second averted their gaze more than children who gave their speech first. Children who gave their speech second displayed less positive affect if their social partner who they watched give a speech first was shyer These findings suggest that preschool-aged children are sensitive to learning about their environment indirectly through social observation.