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Recent evidence from neurophysiology and human functional neuroimaging has given rise to the hypothesis that social, affective touch belongs to a distinct category of tactile experience. Such hedonic and rewarding touch is proposed to operate mainly in the domain of social interactions and relationships. Social touch may play a functional role in the physiological regulation of the body’s responses to acute stressors and other short-term challenges. In this perspective, touch can “buffer” disadvantageous physiological effects of potentially inefficient or maladaptive responses. This review outlines the evidence for such a role, as well as the neural pathways that may support it. Direct evidence for touch as a physiological regulator is strongest for systems that underlie the maintenance of physical proximity to conspecifics in a variety of circumstances. For example, mammalian social physical contact involves social thermoregulatory processes like huddling and snuggling, which also rely on tactile thermosensory and somatosensory pathways. There is also good evidence that touch systems contribute to preventing social separation and facilitating the re-instatement of contact following social separation. Finally, prosocial touch, such as allogrooming and consolation, may utilize some of the same neural pathways as other, non-social means of stress regulation. Social touch may thus serve as part of a system for regulation of responses to acute stressors, “extended” to include the physiological effects of social interactions.

Social thermoregulation is the huddling of two or more individuals that share endogenous warmth to reduce thermoregulation costs. Strategies vary widely depending on the species’ social behavior and the ambient ecological conditions. In greater white-toothed shrews (Crocidura russula), huddling is employed in communal nests only in the colder months, which suggests that temperature is an important factor in the species’ social thermoregulation strategy. To test this hypothesis, we analyzed the behavior and physiology of five groups of shrews from winter, acclimated to 14 °C, and four groups from summer, acclimated to 24 °C. Each group consisted of six captive males that were first housed singly for 2 days and later allowed to interact with other shrews of the same group. Our analysis revealed all group mates were frequently found huddling in the same shelter, regardless of acclimation temperature. However, mass-adjusted resting metabolic rate decreased in winter shrews with larger huddle sizes and remained constant in summer shrews in huddles with three or more individuals. Body temperature was also significantly lower and more varied in winter shrews. After being group-housed, winter shrews used less torpor and significantly increased their body mass and food intake in the first days. Our results suggest that temperature had a small influence in huddling behavior but a large one in physiological factors, such as metabolism, body temperature, and food intake, after shrews started interacting socially. Therefore, social thermoregulation provides benefits to C. russula besides energy savings.

In a prairie vole ( Microtus ochrogaster ) model of social bonding, a functional circuit from the prefrontal cortex to nucleus accumbens is dynamically modulated to enhance females’ affiliative behaviour towards a partner. Social bonding in monogamous voles Most mammalian species do not form monogamous pair-bonds, but the prairie vole is one that does. Oxytocin and dopamine signalling within connected brain areas of the reward-processing network drive social bonding behaviours but the neural mechanisms have been unclear. Here, Robert Liu and colleagues demonstrate that stimulating activity in a connection between the prefrontal cortex and the nucleus accumbens of prairie voles, even in the absence of mating, can bias a female towards a presented partner, suggesting that this connection is not only associated with the formation of social bonds, but can actually enhance it. This reveals how the brain's reward system can be recruited by social interactions to form social bonds. Adult pair bonding involves dramatic changes in the perception and valuation of another individual 1 . One key change is that partners come to reliably activate the brain’s reward system 2 , 3 , 4 , 5 , 6 , although the precise neural mechanisms by which partners become rewarding during sociosexual interactions leading to a bond remain unclear. Here we show, using a prairie vole ( Microtus ochrogaster ) model of social bonding 7 , how a functional circuit from the medial prefrontal cortex to nucleus accumbens is dynamically modulated to enhance females’ affiliative behaviour towards a partner. Individual variation in the strength of this functional connectivity, particularly after the first mating encounter, predicts how quickly animals begin affiliative huddling with their partner. Rhythmically activating this circuit in a social context without mating biases later preference towards a partner, indicating that this circuit’s activity is not just correlated with how quickly animals become affiliative but causally accelerates it. These results provide the first dynamic view of corticostriatal activity during bond formation, revealing how social interactions can recruit brain reward systems to drive changes in affiliative behaviour.

Selective relationships are fundamental to humans and many other animals, but relationships between mates, family members, or peers may be mediated differently. We examined connections between social reward and social selectivity, aggression, and oxytocin receptor signaling pathways in rodents that naturally form enduring, selective relationships with mates and peers (monogamous prairie voles) or peers (group-living meadow voles). Female prairie and meadow voles worked harder to access familiar versus unfamiliar individuals, regardless of sex, and huddled extensively with familiar subjects. Male prairie voles displayed strongly selective huddling preferences for familiar animals, but only worked harder to repeatedly access females versus males, with no difference in effort by familiarity. This reveals a striking sex difference in pathways underlying social monogamy and demonstrates a fundamental disconnect between motivation and social selectivity in males—a distinction not detected by the partner preference test. Meadow voles exhibited social preferences but low social motivation, consistent with tolerance rather than reward supporting social groups in this species. Natural variation in oxytocin receptor binding predicted individual variation in prosocial and aggressive behaviors. These results provide a basis for understanding species, sex, and individual differences in the mechanisms underlying the role of social reward in social preference. What factors drive the formation of social relationships can vary greatly in animals. While some individuals may be motivated to find social partners, others may just tolerate being around others. A desire to avoid strangers may also lead an individual to seek out acquaintances or friends. Sometimes a mix of these factors shape social behavior. Studying motivation for social relationships in the laboratory is tricky. Traditional laboratory animals like mice and rats do not bond with specific peers or mates. But small burrowing rodents called voles are a more relationship-oriented alternative to mice and rats. Prairie voles form selective and enduring preferences for both their mates and familiar same-sex peers. Meadow voles on the other hand, live alone much of the year but move in with other animals over the winter. Beery et al. show that social motivation in voles varies by relationship type, species and sex. In the experiments, voles were first trained to press a lever to get a food reward. Then, the food reward was swapped with access to familiar or unfamiliar voles. Female prairie voles strived to be with animals they knew rather than to be with strangers, while male prairie voles tried hard to access any female. In contrast, meadow voles did not overly exert themselves to access other animals. Beery et al. then measured oxytocin receptor levels in the brains of prairie voles. Prairie voles that had more receptors for oxytocin in part of their brain known as the nucleus accumbens worked harder to access their familiar partner. But individuals with more oxytocin receptors in the bed nucleus of the stria terminalis were more likely to attack an unfamiliar animal. The meadow voles’ behavior suggests that they are more motivated by tolerance of familiar animals, while the female prairie voles may find it rewarding to be with animals they have bonded with. These differences may help explain why these two species of vole have evolved different social behaviors. The experiments also suggest that oxytocin – which is linked with maternal behavior – plays an important role in social motivation. Learning more about the biological mechanisms that underlie vole social behaviors may help scientists identify fundamental aspects of social behavior that may apply to other species including humans.

Despite playing a pivotal role in the inception of animal culture studies, macaque social learning is surprisingly understudied. Social learning is important to survival and influenced by dominance and affiliation in social animals. Individuals generally rely on social learning when individual learning is costly, and selectively use social learning strategies influencing what is learned and from whom. Here, we combined social learning experiments, using extractive foraging tasks, with network-based diffusion analysis (using various social relationships) to investigate the transmission of social information in free-ranging Barbary macaques. We also investigated the influence of task difficulty on reliance on social information and evidence for social learning strategies. Social learning was detected for the most difficult tasks only, with huddling relations outside task introductions, and observation networks during task introductions, predicting social transmission. For the most difficult task only, individuals appeared to employ a social learning strategy of copying the most successful demonstrator observed. Results indicate that high social tolerance represents social learning opportunities and influences social learning processes. The reliance of Barbary macaques on social learning, and cues of model-success supports the costly information hypothesis. Our study provides more statistical evidence to the previous claims indicative of culture in macaques.

Social isolation affects the brain and behavior in a variety of animals, including humans. Studies in traditional laboratory rodents, including mice and rats, have supported the idea that short-term social isolation promotes affiliative social behaviors, while long-term isolation promotes anti-social behaviors, including increased aggression. Whether the effects of isolation on the social behaviors of mice and rats generalize to other rodents remains understudied. In the current study, we characterized the effects of short-term (3-days) social isolation on the social behaviors of adult prairie voles ( Microtus ochrogaster ) during same-sex and opposite-sex social interactions. Our experiments revealed that short-term isolation did not affect rates of ultrasonic vocalizations or time spent in non-aggressive social behaviors and huddling during same-sex and opposite-sex interactions. Unexpectedly, although short-term isolation also did not affect time spent in resident-initiated and mutually-initiated aggressive behavior, we found that short-term isolation increased time spent in visitor-initiated aggression during male-male interactions. Our findings highlight the importance of comparative work across species and the consideration of social context to understand the diverse ways in which social isolation can impact social behavior.

The rapid decrease of light intensity is a potent stimulus of rats’ activity. The nature of this activity, including the character of social behavior and the composition of concomitant ultrasonic vocalizations (USVs), is unknown. Using deep learning algorithms, this study aimed to examine the social life of rat pairs kept in semi-natural conditions and observed during the transitions between light and dark, as well as between dark and light periods. Over six days, animals were video- and audio-recorded during the transition sessions, each starting 10 minutes before and ending 10 minutes after light change. The videos were used to train and apply the DeepLabCut neural network examining animals’ movement in space and time. DeepLabCut data were subjected to the Simple Behavioral Analysis (SimBA) toolkit to build models of 11 distinct social and non-social behaviors. DeepSqueak toolkit was used to examine USVs. Deep learning algorithms revealed lights-off-induced increases in fighting, mounting, crawling, and rearing behaviors, as well as 22-kHz alarm calls and 50-kHz flat and short, but not frequency-modulated calls. In contrast, the lights-on stimulus increased general activity, adjacent lying (huddling), anogenital sniffing, and rearing behaviors. The animals adapted to the housing conditions by showing decreased ultrasonic calls as well as grooming and rearing behaviors, but not fighting. The present study shows a lights-off-induced increase in aggressive behavior but fails to demonstrate an increase in a positive affect defined by hedonic USVs. We further confirm and extend the utility of deep learning algorithms in analyzing rat social behavior and ultrasonic vocalizations.

Background Huddling is highly evolved as a cooperative behavioral strategy for social mammals to maximize their fitness in harsh environments. Huddling behavior can change psychological and physiological responses. The coevolution of mammals with their microbial communities confers fitness benefits to both partners. The gut microbiome is a key regulator of host immune and metabolic functions. We hypothesized that huddling behavior altered energetics and thermoregulation by shaping caecal microbiota in small herbivores. Brandt’s voles ( Lasiopodomys brandtii ) were maintained in a group (huddling) or as individuals (separated) and were exposed to warm (23 ± 1 °C) and cold (4 ± 1 °C) air temperatures ( T a ). Results Voles exposed to cold T a had higher energy intake, resting metabolic rate (RMR) and nonshivering thermogenesis (NST) than voles exposed to warm T a . Huddling voles had lower RMR and NST than separated voles in cold. In addition, huddling voles had a higher surface body temperature ( T surface ), but lower core body temperature ( T core ) than separated voles, suggesting a lower set-point of T core in huddling voles. Both cold and huddling induced a marked variation in caecal bacterial composition, which was associated with the lower T core . Huddling voles had a higher α and β-diversity, abundance of Lachnospiraceae and Veillonellaceae , but lower abundance of Cyanobacteria , Tenericutes , TM7, Comamonadaceae , and Sinobacteraceae than separated voles. Huddling or cold resulted in higher concentrations of short-chain fatty acids (SCFAs), particularly acetic acid and butyric acid when compared to their counterparts. Transplantation of caecal microbiota from cold-separated voles but not from cold-huddling voles induced significant increases in energy intake and RMR compared to that from warm-separated voles. Conclusions These findings demonstrate that the remodeling of gut microbiota, which is associated with a reduction in host T core , mediates cold- and huddling-induced energy intake and thermoregulation and therefore orchestrates host metabolic and thermal homeostasis. It highlights the coevolutionary mechanism of host huddling and gut microbiota in thermoregulation and energy saving for winter survival in endotherms.

Animals of large group-living species that exhibit dispersal or have overlapping territories with other groups frequently encounter novel conspecifics. To avoid injury, successfully obtain a mate, integrate into a new group, and/or to determine one’s social rank, it is crucial to accurately assess social information. The lateral hypothalamus (LH) is critical for learning about food-related cues and shifting behavior toward or away from salient events. While the LH facilitates risk assessment in dyadic social competitions, how the LH modulates social behavior in non-aggressive contexts with novel peers remains unknown. In the highly colonial spiny mouse ( Acomys dimidiatus ), we used chemogenetics to inhibit the LH of females as they interacted with novel peers in a novel vs. familiar preference test, a group size preference test, and a group interaction test. Although control females were investigative and prosocial (e.g., affiliative proximity), they exhibited significant social avoidance of a novel peer group. However, we found that inhibition of the LH induced a preference for social novelty, decreased social avoidance, and promoted affiliative proximity and huddling with a novel, previously established group of peers. These findings suggest that the LH may function to promote cautious behavior, potentially via risk assessment, in novel social environments.

Australian funnel-web spiders are iconic species, characterized as being the most venomous spiders in the world. They are also valued for the therapeutics and natural bioinsecticides potentially hidden in their venom molecules. Although numerous biochemical and molecular structural approaches have tried to determine the factors driving venom complexity, these approaches have not considered behaviour, physiology and environmental conditions collectively, which can play a role in the evolution, complexity, and function of venom components in funnel-webs. This study used a novel interdisciplinary approach to understand the relationships between different behaviours (assessed in different ecological contexts) and morphophysiological variables (body condition, heart rate) that may affect venom composition in four species of Australian funnel-web spiders. We tested defensiveness, huddling behaviour, frequency of climbing, and activity for all species in three ecological contexts: i) predation using both indirect (puff of air) and direct (prodding) stimuli; ii) conspecific tolerance; and iii) exploration of a new territory. We also assessed morphophysiological variables and venom composition of all species. For Hadronyche valida , the expression of some venom components was associated with heart rate and defensiveness during the predation context. However, we did not find any associations between behavioural traits and morphophysiological variables in the other species, suggesting that particular associations may be species-specific. When we assessed differences between species, we found that the species separated out based on the venom profiles, while activity and heart rate are likely more affected by individual responses and microhabitat conditions. This study demonstrates how behavioural and morphophysiological traits are correlated with venom composition and contributes to a broader understanding of the function and evolution of venoms in funnel-web spiders.