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Social interactions are often analyzed by scoring segments of predefined behavior and then statistically assessing numerical and sequential patterns to identify the structure of the encounters. However, this approach can miss the dynamics of the animals' relationship over the course of the encounter, one that often involves invariant bonds, say a nose-to-nose orientation, with many different movements performed by both partners acting to counteract each other's attempts to break or maintain the relationship. Moreover, these invariant bonds can switch from one configuration to another during an interaction, leading from one stable configuration to another. It is this stepwise sequence of configurational stabilities that lead to functional outcomes, such as mating, aggression, or predation. By focusing on the sequence of invariant relational configurations, the deep structure of interactions can be discerned. This deep structure can then be used to differentiate between compensatory movements, no matter how seemingly stereotyped they may appear, from movement patterns which are restricted to a particular form when more than one option is available. A dynamic perspective requires suitable tools for analysis, and such tools are highlighted as needed in describing particular interactions., Competing Interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision., (Copyright © 2024 Ham, Pellis and Pellis.)

Play behavior is typically most frequent in immature animals and then declines by adulthood. New research reveals a brain mechanism that may underlie this age-related decline in play., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2024 Elsevier Inc. All rights reserved.)

Like many mammals, as juveniles, rats engage in play fighting, which in the laboratory is typically studied in dyads, and consequently, it is the researcher who determines a rat's play partner. In real-life conditions, a rat would have many partners with whom to play. In a previous study, we found that rats do prefer to play with some individuals more than others, and surprisingly, when given the choice, unfamiliar partners are preferred to familiar ones. In this study, we assessed partner choice when all the available partners are strangers. Eight groups of six unfamiliar juvenile male rats were observed for 10 min play trials. One of the six in each group was selected as the 'focal' rat and his play towards, and received by, the others were scored. Social networks revealed that five of the eight groups formed preferences, with preferred partners also engaging in more play with the focal rat. The mechanism by which these preferences were formed remains to be determined, but it seems that there are individual differences, potentially in the amount and style of play, that allow an individual to select the most suitable partner from a group of strangers., (© 2024. The Author(s).)

The nature of play in animals has been long debated, but progress is being made in characterizing play and its variants, documenting its distribution across vertebrate and invertebrate taxa, describing its mechanisms and development, and proposing testable theories about its origins, evolution, and adaptive functions. To achieve a deeper understanding of the functions and evolution of play, integrative and conceptual advances are needed in neuroscience, computer modeling, phylogenetics, experimental techniques, behavior development, and inter- and intra-specific variation. The special issue contains papers documenting many of these advances. Here, we describe seven timely areas where further research is needed to understand this still enigmatic class of phenomena more fully. Growing empirical and theoretical evidence reveals that play has been crucial in the evolution of behavior and psychology but has been underestimated, if not ignored, in both empirical and theoretical areas of evolutionary biology and neuroscience. Play research has important ramifications for understanding the evolution of cognition, emotion, and culture, and research on animals can be both informative and transformative., (Crown Copyright © 2024. Published by Elsevier Ltd. All rights reserved.)

Reduced play experience over the juvenile period leads to adults with impoverished social skills and to anatomical and physiological aberrations of the neurons found in the medial prefrontal cortex (mPFC). Even rearing rats from high-playing strains with low-playing strains show these developmental consequences. In the present study, we evaluated whether low-playing rats benefit from being reared with higher playing peers. To test this, we reared male Fischer 344 rats (F344), typically thought to be a low-playing strain, with a Long-Evans (LE) peer, a relatively high-playing strain. As juveniles, F344 rats reared with LE rats experienced less play and lower quality play compared to those reared with another F344. As adults, the F344 rats reared with LE partners exhibited poorer social skills and the pyramidal neurons of their mPFC had larger dendritic arbors than F344 rats reared with same-strain peers. These findings show that being reared with a more playful partner does not improve developmental outcomes of F344 rats, rather the discordance in the play styles of F344 and LE rats leads to poorer outcomes., (© 2024 The Authors. Developmental Psychobiology published by Wiley Periodicals LLC.)

Belugas (Delphinapterus leucas) engage in many forms of play (e.g., object, water, locomotor), but no play is quite as curious as the unusual form of cooperative social play involving mouth-to-mouth interactions. These playful interactions are characterized by two belugas approaching each other head-to-head and interlocking their jaws, clasping one another, as if they were shaking hands. Observed in belugas both in the wild and in managed care, it is seemingly an important type of social play that offers a unique way of socializing with conspecifics. To describe this unusual behavior, a group of belugas in managed care was observed from 2007 to 2019. Although adults participated in mouth-to-mouth interactions, most were initiated and received by young belugas. Both males and females engaged in mouth-to-mouth interactions and did so at similar frequencies. Individual differences in how many mouth-to-mouth interactions were initiated among calves were also observed. Due to the unique, cooperative nature of mouth-to-mouth interactions, which require both social and motor skills, it is hypothesized that these interactions may be used to test social and motor competency., (© 2023 The Authors. Zoo Biology published by Wiley Periodicals LLC.)

Social play in rats is rewarding and important for the development of brain and social skills. There are differences in the amount of play behavior displayed among individuals, with earlier studies suggesting that, despite variation across trials, individual differences tend to be consistent. In the present study, juvenile Lister-hooded rats were paired with a different, unfamiliar same-sex partner on three days and based on the amount of play each individual initiated, it was characterized as a high, medium or low player. Using this categorization, we explored three features related to individual differences. First, we show that by increasing the number of test days from two, as was done in a previous study (Lesscher et al., 2021), to three, characterization was effectively improved. Secondly, while the earlier study only used males, the present study showed that both sexes exhibit a similar pattern of individual differences in the degree of playfulness. Even though low players consistently initiated less play than medium and high players, all rats varied in how much play they initiated from one trial to the next. Thirdly, we assessed two potential mechanisms by which the playfulness of one rat can modify the level of playfulness of the other rat (i.e., emotional contagion vs homeostasis). Analyses of individuals' contribution to the play of dyads suggest that rats consistently adjust their play behavior depending on the behavior displayed by the partner. Since this adjustment can be positive or negative, our data support a homeostatic mechanism, whereby individuals increase or decrease the amount of play they initiate, which results in the experience of an overall stable pattern of play across trials. Future research will investigate the neural bases for individual differences in play and how rats maintain a preferred level of play., Competing Interests: Declaration of Competing Interest Apart from funding received from the mentioned grants, the authors declare no conflict of interest., (Copyright © 2023 The Authors. Published by Elsevier B.V. All rights reserved.)

Self-handicapping behaviors evolved as honest signals that reliably reflect the quality of their performers. In playful activities, self-handicapping is described as intentionally and unnecessarily putting oneself into disadvantageous positions and situations. Self-handicapping during play may allow individuals to learn to cope with unexpected events by improving sensori-motor coordination, as well as function as a play solicitation signal. One such self-handicapping behavior involves moving about while deliberately covering one's eyes. We conducted a quantitative study of object-assisted eye-covering (OAEC) in a population of free-ranging Balinese macaques. After evaluating the frequency, form, distribution, and context of OAEC, we measured the responses this behavior elicited (1) in the performers with a focus on sensori-motor self-handicapping, and (2) in their conspecifics, with an emphasis on whether, and if so how, OAEC may facilitate social play. Our data provided some support for several hypotheses: OAEC is a sensori-motor self-handicapping behavior, an attention-getting cue, a social play signal, and a socially self-handicapping tactic during social play. We discuss our results from the perspective of tool-assisted self-handicapping behavior, propose a scenario to account for the emergence of this behavioral innovation, and speculate on the cultural nature of OAEC., (© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)

In rats reared without play, or with limited access to play during the juvenile period, the dendrites of pyramidal neurons of the medial prefrontal cortex (mPFC) exhibit more branching than rats reared with more typical levels of play. This suggests that play is critical for pruning the dendritic arbor of these neurons. However, the rearing paradigms typically used to limit play involve physical separation from a peer or sharing a cage with an adult, causing stress that may disrupt pruning. To limit this potentially confounding source of stress, we used an alternative approach in this study: pairing playful Long Evans rats (LE) with low playing Fischer 344 (F344) rats throughout the juvenile period. We then examined the morphology of medial prefrontal cortex (mPFC) neurons, predicting that pruning should be reduced. LE rats reared with another LE rat had significantly greater pruning of mPFC pyramidal neurons compared to LE rats reared with a F344 partner. Furthermore, in previous studies, only one sex or the other was used, whereas in the present rearing paradigm, both sexes were tested, showing that play influences neuronal pruning in both. The neurons of the play deficient LE rats not only occupied more space, as determined by convex hull analyses, but the dendrites were also longer than in rats with more typical play experiences. Unlike studies using more stressful rearing paradigms, the present effects were limited to the apical dendritic projections, suggesting that the previously reported effects on the basilar dendrites may have resulted from developmental disruptions caused by stress. If correct, the present findings indicate that play experienced over the juvenile period affects how mPFC neurons develop and function., (Copyright © 2022 Elsevier B.V. All rights reserved.)

The benefits gained by young animals engaging in play fighting have been a subject of conjecture for over a hundred years. Progress in understanding the behavioral development of play fighting and the underlying neurobiology of laboratory rats has produced a coherent model that sheds light on this matter. Depriving rats of typical peer-peer play experience during the juvenile period leads to adults with socio-cognitive deficiencies and these are correlated with physiological and anatomical changes to the neurons of the prefrontal cortex, especially the medial prefrontal cortex. Detailed analysis of juvenile peer play has shown that using the abilities needed to ensure that play fighting is reciprocal is critical for attaining these benefits. Therefore, unlike that which was posited by many earlier hypotheses, play fighting does not train specific motor actions, but rather, improves a skill set that can be applied in many different social and non-social contexts. There are still gaps in the rat model that need to be understood, but the model is well-enough developed to provide a framework for broader comparative studies of mammals from diverse lineages that engage in play fighting., (Copyright © 2023 Elsevier Ltd. All rights reserved.)

Social play in rats is a highly rewarding, energetic form of social interaction and important for development of the brain and social skills. The 50 kHz ultrasonic vocalizations (USV) emitted during social play are thought to be an expression of a positive affective state (laughter), which in some situations may also function as communication signals. Heterospecific play, 'tickling' by an experimenter, is thought to simulate conspecific play, and has been used to improve welfare and to study the neurobiology of positive affect. Given that tickling evokes substantial amounts of USV, we investigated whether heterospecific play is simulating conspecific play by comparing USV-behaviour associations in both contexts. If the 50 kHz calls are merely an expression of 'laughter' then the pattern and type of emission in both contexts should be similar. By contrast, as playing with a conspecific involves a two-way exchange of signalling, the additional demands on communication should lead to a different pattern of calling. While calling was prevalent in both types of play, how the different types of 50 kHz calls are used in the two contexts differed markedly. The findings suggest that while conspecific and heterospecific play are positive experiences, tickling is not the equivalent of conspecific play. This article is part of the theme issue 'Cracking the laugh code: laughter through the lens of biology, psychology and neuroscience'.

Competing Interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

While the ontogeny of beluga (Delphinapterus leucas) socio-sexual behavior has been documented in animals between 37- and 108-months-old, the first 36 months of life are yet to be examined. This study investigated how socio-sexual behaviors emerge over the first three years of life in a group of belugas in managed care. The emergence of socio-sexual behaviors was relatively consistent among immature animals. More complex behaviors, like s-posture presentations, developed in a piecemeal fashion (i.e., simple components of the behavior sequence emerged before complex components). The presence of an adult male significantly predicted if immature belugas would initiate and participate in socio-sexual behavior. However, partner preferences changed with age. In the first year of life, belugas engaged in sexual behavior with their mother most frequently but preferred to play with older males if given a choice. By the third year of life, belugas engaged in socio-sexual behavior most frequently with other immature animals. These findings enhance our understanding of how belugas develop sexually and socially and have implications for social housing practices of immature belugas., (Copyright © 2022 Elsevier B.V. All rights reserved.)

Rough-and-tumble play or play fighting is an important experience in the juvenile period of many species of mammals, as it facilitates the development of social skills, and for some species, play fighting is retained into adulthood as a tool for assessing and managing social relationships. Laboratory rats have been a model species for studying the neurobiology of play fighting and its key developmental and social functions. However, play fighting interactions are complex, involving competition and cooperation; therefore, no single measure to quantify this behavior is able to capture all its facets. Therefore, in this paper, we present a multilayered framework for scoring all the relevant facets of play that can be affected by experimental manipulations and the logic of how to match what is measured with the question being asked. © 2022 Wiley Periodicals LLC., (© 2022 Wiley Periodicals LLC.)

Rats reared with limited access to a play partner during the juvenile period develop into adults with impairments in various cognitive, emotional, and social skills. The present study assesses the consequences of play deprivation on adult social skills in female Long Evans (LE) rats that were reared with a low-playing Fischer 344 rat over the juvenile period. As adults, their social skills were assessed using the stranger paradigm, by pairing the deprived LE rats with a novel LE partner in a neutral arena. While the deprived rat engages its partner in play there were alterations in key aspects of play, such as reduced pinning and a longer latency to begin playing, that suggest there are impairments in the social ability of the deprived rat. Most notable were the changes in the behaviour of the typically reared partner, a reduction in the amount of play it initiated and fewer actions that produced reciprocal and prolonged interactions. The changes in the behaviour of the normally reared partner suggest that it detected subtle changes in the play deprived LE rats. These findings support the hypothesis that peer-peer play experiences during the juvenile period are important for the development of socio-cognitive skills., (Copyright © 2021 Elsevier B.V. All rights reserved.)

The epileptogenic-prone (FAST) and epileptogenic-resistant (SLOW) rat strains have become a valuable tool for investigating neural plasticity. The strains were generated by breeding the rats that required the fewest amygdala stimulations to elicit a stage-5 convulsive seizure (FAST) and rats requiring the most stimulations (SLOW). Previous studies have shown differences in behavior and amygdala physiology in the two strains. This study examined the dendritic morphology of pyramidal neurons in the brains of adult male and female rats of the two strains. The brains were stained with the Golgi-Cox method and the length and branching from layer III pyramidal cells were measured in parietal cortex (Zilles Par1), medial frontal cortex (Zilles Cg3), and orbitofrontal cortex (Zilles AID) in these two strains of rats. We observed significantly longer dendrites in Cg3 in the FAST group but longer dendrites in the SLOW group in AID and Par1. There was also a sex difference (M > F) in Par1 in both strains. These morphological differences can provide insights into the neurobiological basis of the behavioral differences and suggest that localized changes in the amygdala do not occur independently of changes in other brain regions, and especially prefrontal cortex., (© 2021 Wiley Periodicals LLC.)

Rats emit a variety of calls in the 40-80 kHz range (50 kHz calls). While these calls are generally associated with positive affect, it is unclear whether certain calls might be used selectively in certain contexts. To examine this, we looked at ultrasonic calls in 30-40 day old male rats during the expectation of either play or food, both of which are reinforcing. Behavior and vocalizations were recorded while rats were in a test chamber awaiting the arrival of a play partner or food over seven days of testing. Control groups were included for the non-specific effects of food deprivation and social isolation. Play reward led to an increase in 50 kHz vocalizations, generally, with specific increases in trill and "trill with jump" calls not seen in other groups. Expectation of food reward did not lead to a significant increase in vocalizations of any type, perhaps due to the young age of our study group. Further, rats that were food deprived for the food expectation study showed markedly lower calls overall and had a different profile of call types compared to rats that were socially isolated. Taken together, the results suggest that trill-associated calls may be used selectively when rats are socially isolated and/or expecting a social encounter.

Object affordances play a major role in action expression: (a) providing opportunities to generate potential solutions to instrumental problems and (b) shaping and constraining the motor actions available to an individual. The playful manipulation of objects can facilitate individual acquisition of functional object-assisted actions through affordance learning. We tested the "object affordance" hypothesis in free-ranging long-tailed macaques. This hypothesis holds that the physical properties associated with stone size afford different stone-directed actions, in the context of stone handling (SH) behavior, a form of culturally maintained stone play from which stone tool use can emerge. We predicted that higher SH versatility (i.e., total number of different SH behavioral elements expressed) and higher duration of the SH behavioral element "Pound" would be associated with the manipulation of medium-sized stones, followed by small stones, and then large stones. Our data partly supported these predictions. Both medium-sized and small-sized stones afforded the highest SH versatility, and a higher duration of "Pound" than large stones. As expected, duration of "Pound" was higher with medium than small stones, but the difference was not statistically significant. Our results were consistent with Newell's constraint model, which emphasizes the role of objects' physical properties in limiting and enhancing the expression of actions directed to these objects. The relaxed selective pressures acting on SH behavior may enhance the expression of a range of actions directed toward stones of different sizes that could facilitate the emergence of instrumental solutions and may contribute to explaining the evolution of lithic technology in early humans. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Hand use is a widespread act in many vertebrate lineages and subserves behaviors including locomotion, predation, feeding, nest construction, and grooming. In order to determine whether hand use is similarly used in social behavior, the present paper describes hand use in the social play of rats. In the course of rough and tumble play sessions, rats are found to make as many as twenty different movements a minute with each hand for the purposes of manipulating a partner into a subordinate position or defending against a partner's attack. The hand movements comprise signaling movements of touching, offensive manipulating of a partner to control a play engagement, and defensive hand movements directed toward blocking, pushing and pulling to parry an attack. For signaling, attack and defense, hand movements have a structure that is similar to the structure of hand movements used for other purposes including eating, but in their contact points on an opponent, they are tailored for partner control. Given the time devoted to play by rats, play likely features the social rat behavior with the most extensive use of hand movements. This extensive use of hand movements for social play is discussed in relation to the ubiquity of hand use in adaptive behavior, the evolution of hand use in the play of mammals, and in relation to extending the multifunctional theory of the purposes of play to include the education of skilled hand movements for various adult functions including as feeding., (© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)

The Wistar-Kyoto (WKY) rat was developed as a control for the spontaneous hypertensive rat but has subsequently also been used as a genetic animal model of depression due to its hyper-responsiveness to stress. We used anticipation of social reward (i.e., a play partner) to assess behavioural and vocal differences between the WKY and normal Wistar (WI) rats in the juvenile period. We found marked differences between groups; the WKY rats, were less active, vocalized less, and used significantly fewer types of 50-kHz calls in comparison to their WI counterparts. The animals were re-tested in adulthood and the same differences existed in overall activity, types of vocalizations and the behavioural vocal profiles used by the two groups of animals. These findings provide a robust baseline for an animal model of depression using a social paradigm. This paradigm may be useful to evaluate the efficacy of pharmaceutical interventions as potential treatments of depression in WKY rats., (Copyright © 2020 Elsevier B.V. All rights reserved.)

Inferring functional components of behavioral sequences is a crucial but challenging task. A systematic comparison of their temporal structure is a good starting point, based on the postulate that more functional traits are less structurally variable. We studied stone handling behavior (SH) in Balinese long-tailed macaques, a versatile form of stone-directed play. We tested the hypothesis that stones are used by male monkeys to stimulate their genitals in a sexual context (i.e., "sex toy" hypothesis). Specifically, two SH actions (i.e., "tap-on-groin" (TOG) and "rub-on-groin" (ROG), respectively the repetitive tapping and rubbing of a stone onto the genital area) gained functional properties as self-directed tool-assisted masturbation. Owing to the structural organization of playful activities, we predicted that SH sequences without TOG/ROG would exhibit higher levels of variability, repeatability and exaggeration than SH sequences with TOG/ROG. We also predicted that TOG/ROG would occur more often and last longer in SH sequences in which penile erection - a sexually-motivated physiological response in primates - was observed than in SH sequences in which penile erection was not observed. To identify and compare recurring series of SH patterns otherwise undetectable by using conventional quantitative approaches across SH sequences containing TOG/ROG or not, we used a temporal analysis known as "T-pattern detection and analysis" (TPA). Our predictions about variability, exaggeration and temporal association between TOG/ROG in males and penile erection were supported. As expected, SH sequences without TOG/ROG were, on average, more repeatable than SH sequences with TOG/ROG, but the difference was not statistically significant. Overall, the "sex toy" hypothesis was partly supported, and our results suggested that TOG and ROG are two forms of tool-assisted genital stimulation, possibly derived from the playful handling of stones. These findings are consistent with the view that tool use may evolve in stages from initially non-functional object manipulation, such as object play., (Copyright © 2020 Elsevier Inc. All rights reserved.)

Ultrasonic vocalizations (USVs) emitted by rat pups have been extensively studied in the context of isolation from their mother and littermates. The heightened call rate of isolation-induced USVs indicates increased anxiety, whereas other acoustic parameters, such as frequency and call duration, are thought to be useful in reflecting developmental changes, which by weaning have developed into their adult form. However, it is possible that stress can affect the quality as well as the quantity of calls, and that as the pups become more mobile, the effects of the stress may change. Therefore, in the present study rats were tested in a test arena either in isolation or with littermates, so as to assess the effects of isolation stress on the developmental changes reported in the literature. Rat pups of both sexes were tested on multiple days from postnatal day (PND) 7 to weaning. Overall, the main changes in the frequency, duration, and types of calls were accounted for by age. The effects of isolation were minor, as were sex differences. This study indicates that the development of USVs in infant rats is a robust process and seemingly resistant to the effects of isolation-induced stress., (© 2019 Wiley Periodicals, Inc.)

Structural modifications in the dendritic morphology of neurons occur following many forms of experience, including exposure to drugs, complex housing, and training in specific behavioral tasks. The present study examined morphological changes in orbitofrontal (OFC) and medial prefrontal cortex (mPFC) neurons of female rats following experience with a variety of social partners or nonsocial olfactory stimuli. We reasoned that experience with various social partners or olfactory stimuli, and the associated behavioral adaptations, would drive structural modifications in prefrontal cortex neurons engaged by these stimuli. Social experience was manipulated by providing rats with a novel cage-mate or housing the animal with the same cage-mate throughout the study. Similarly, olfactory experience was manipulated by introducing novel, nonsocial odors in the home cage or exposing the animals to the same home-cage odor throughout the study. Both forms of experience resulted in altered dendritic morphology in OFC neurons, whereas morphological changes in mPFC were comparatively small and limited to changes in spine density. These observations indicate that OFC and mPFC neurons respond differently to social and nonsocial olfactory stimulation in adulthood and join the growing body of data illustrating differential effects of experience on structural plasticity in OFC and mPFC. (PsycINFO Database Record (c) 2020 APA, all rights reserved).

Given that many behavior patterns cluster together in sequences that are organized to solve specific problems (e.g., foraging), a fruitful perspective within which to study behaviors is as distinct 'behavior systems'. Unlike many behavior systems that are widespread (e.g., anti-predator behavior, foraging, reproduction), behavior that can be relegated as playful is diverse, involving behavior patterns that are typically present in other behavior systems, sporadic in its phylogenetic distribution and relatively rare, suggesting that play is not a distinct behavior system. Yet the most striking and complex forms of play have the organizational integrity that suggests that it is a behavior system. One model that we develop in this paper, involves three stages of evolutionary transition to account for how the former can evolve into the latter. First, play-like behavior emerges from the incomplete development of other, functional behavior systems in some lineages. Second, in some of those lineages, the behavior patterns typical of particular behavior systems (e.g., foraging) are reorganized, leading to the evolution of specific 'play behavior systems'. Third, some lineages that have independently evolved more than one such play behavior system, coalesce these into a 'super system', allowing some animals to combine behavior patterns from different behavior systems during play. Alternative models are considered, but irrespective of the model, the overall message from this paper is that the conceptual framework of the behavior system approach can provide some new insights into the organization and diversity of play present in the animal kingdom., (Copyright © 2019 The Authors. Published by Elsevier B.V. All rights reserved.)

Juvenile animals of many species engage in social play, but its functional significance is not well understood. This is especially true for a type of social play called fair play (Fp). Social play often involves behavioral patterns similar to adult behaviors (e.g., fighting, mating, and predatory activities), but young animals often engage in Fp behaviors such as role-reversals and self-handicapping, which raises the evolutionary problem of why Fp exists. A long-held working hypothesis, tracing back to the 19th century, is that social play provides contexts in which adult social skills needed for adulthood can be learned or, at least, refined. On this hypothesis, Fp may have evolved for adults to acquire skills for behaving fairly in the sense of equitable distribution of resources or treatment of others. We investigated the evolution of Fp using an evolutionary agent-based model of populations of social agents that learn adult fair behavior (Fb) by engaging in Fp as juveniles. In our model, adults produce offspring by accumulating resources over time through foraging. Adults can either behave selfishly by keeping the resources they forage or they can pool them, subsequently dividing the pooled resources after each round of foraging. We found that fairness as equitability was beneficial especially when resources were large but difficult to obtain and led to the evolution of Fp. We conclude by discussing the implications of this model, for developing more rigorous theory on the evolution of social play, and future directions for theory development by modeling the evolution of play.

Juvenile social interactions have been shown to influence the dendritic complexity of neurons in the prefrontal cortex (PFC). In particular, social play induces pruning of the cells in the medial prefrontal cortex (mPFC), whereas interacting with multiple partners, whether those interactions involve play or not, increases the complexity of cells in the orbital frontal cortex (OFC). Previous studies suggest that these changes differ in their stability during adulthood. In the present study, rats were reared in groups of either four (quads) or two (pairs) and the brains of the rats from each rearing condition were then harvested at 60 days (i.e., shortly after sexual maturity) and 100 days (i.e., fully adult). The rats housed with multiple partners had more complex neurons of the OFC at 60 days and this complexity declined to a comparable level to that of pair housed rats by 100 days. In contrast, the play-induced changes of the mPFC remained similar at both ages. These findings suggest that the changes in the PFC induced by different social experiences in the juvenile period differ in how long they are maintained in adulthood. Differences in the functions regulated by the OFC and the mPFC are considered with regard to these differences in the stability of juvenile-induced neural changes., (© 2017 Wiley Periodicals, Inc.)

Play fighting is a commonly reported form of play that involves competitive interactions that generally do not escalate to serious fighting. Although in many species what are competed over are the body targets that are bitten or struck in serious fighting, for many others, the competition can be over other forms of contact, such as sex, social grooming, and predation. In primates, the most detailed studies have been of species such as Old World monkeys, that engage in play fighting that simulates serious fighting, but reports of a number of others, especially among nocturnal prosimians, have noted that play fighting can also involve simulation of sex and grooming. The present study on captive born gray mouse lemurs ( Microcebus murinus ) provides a quantitative assessment of the relative engagement by juveniles in play fighting involving agonistic and amicable targets. About 80% of play fighting involves competing to groom or mount one another, with a minority involving competing to bite. That these forms of play fighting may be distinct from one another is suggested by the finding that attack on one target does not lead to counterattack on another. The findings are discussed in terms of the evolution and mechanisms underlying play fighting in primates and more widely among animals. (PsycINFO Database Record, ((c) 2018 APA, all rights reserved).)

Play fighting is a common form of play reported among species of mammals, birds, and some other taxa. The competition present in play fighting revolves around gaining some advantage, such as biting a partner without being bitten. The behavior simulated during play fighting need not be restricted to that present in adult serious fighting, but can involve competitive interactions derived from amicable behavior, such as sex and social grooming, or from nonsocial competition, such as predation. What unifies play fighting, irrespective of the functional behavior being simulated, is that it involves some degree of reciprocity, or turn taking, that requires that the competition be attenuated by cooperation. However, there are several different ways in which cooperation can be inserted into playful interactions, and these vary in use across different species. The moderation of competition with cooperation forces animals to monitor their own actions and those of their partners, and this common feature appears to be one vehicle through which the experience of play fighting in the juvenile period can train animals for greater psychological resilience. The monitoring and contextual adjustment of actions influences the development of executive functions of the brain, which, in turn, leads to the development of more adaptable adults.

Play fighting is most commonly associated with juvenile animals, but in some species, including rats, it can continue into adulthood. Post-pubertal engagement in play fighting is often rougher and has an increased chance of escalation to aggression, making the use of play signals to regulate the encounter more critical. During play, both juvenile and adult rats emit many 50-kHz calls and some of these may function as play facilitating signals. In the present study, unfamiliar adult male rats were introduced in a neutral enclosure and their social interactions were recorded. While all pairs escalated their playful encounters to become rougher, only the pairs in which one member was devocalized escalated to serious biting. A Monte Carlo shuffling technique was used for the analysis of the correlations between the overt playful and aggressive actions performed and the types and frequencies of various 50-kHz calls that were emitted. The analysis revealed that lower frequency (20-30kHz) calls with a flat component maybe particularly critical for de-escalating encounters and so allowing play to continue. Moreover, coordinating calls reciprocally, with either the same call mimicked in close, temporal association or with complementary calls emitted by participants as they engage in complementary actions (e.g., attacking the nape, being attacked on the nape), appeared to be ways with which calls could be potentially used to avoid escalation to aggression and so sustain playful interactions., (Copyright © 2017 Elsevier B.V. All rights reserved.)

Rat ultrasonic vocalizations have been suggested to be either a byproduct of physical movement or, in the case of 50-kHz calls, a means to communicate positive affect. Yet there are up to 14 distinct types of 50-kHz calls, raising issues for both explanations. To discriminate between these theories and address the purpose for the numerous 50-kHz call types, we studied single juvenile rats that were waiting to play with a partner, a situation associated with a high number of 50-kHz calls. We used a Monte-Carlo shuffling procedure to identify vocalization-behavior correlations that were statistically different from chance. We found that certain call types ("split", "composite" and "multi-step") were strongly associated with running and jumping while other call types (those involving "trills") were more common during slower movements. Further, non-locomotor states such as resting and rearing were strongly predictive of a lack of vocalizations. We also found that the various sub-types of USVs can be clustered into 3-4 categories based on similarities in the way they are used. We did not find a one-to-one relationship between any movements and specific vocalizations, casting doubt on the motion byproduct theory. On the other hand, the use of specific calls during specific behaviors is problematic for the affect communication hypothesis. Based on our results, we suggest that ultrasonic calls may serve to coordinate moment-to-moment social interactions.

Negative social experiences during adolescence are central features for several stress-related mental illnesses. Social play fighting behavior in rats peaks during early adolescence and is essential for the final maturation of brain and behavior. Manipulation of the rat adolescent social experience alters many neurobehavioral measurements implicated in anxiety, depression, and substance abuse. In this review, we will highlight the importance of social play and the use of three separate social stress models (isolation-rearing, social defeat, and social instability stress) to disrupt the acquisition of this adaptive behavior. Social stress during adolescence leads to the development of anxiety and depressive behavior as well as escalated drug use in adulthood. Furthermore, sex- and age-dependent effects on the hormonal stress response following adolescent social stress are also observed. Finally, manipulation of the social experience during adolescence alters stress-related neural circuits and monoaminergic systems. Overall, positive social experiences among age-matched conspecifics during rat adolescence are critical for healthy neurobehavioral maturation., (Copyright © 2017 Elsevier Ltd. All rights reserved.)

When rats engage in playful interactions, they emit appetitive 50-kHz ultrasonic vocalizations (USVs). We investigated the role of 50-kHz USVs in the playful behavior of both juvenile and adult rats. A cohort of juvenile rats was surgically devocalized and allowed to interact with either devocalized or intact partners as juveniles and again as adults. A substantial decrease in playful motivation was seen for pairs of devocalized rats, as well as all intact rats housed with devocalized ones. In pairs in which at least one partner could vocalize, there was no difference in the number of playful interactions as compared to controls. Further investigation revealed that, within the playful episode itself, 50-kHz USVs are more likely to appear before a playful attack is launched than after, regardless of the attacking partner's ability to vocalize, and when one partner is pinned on its back by another, it is the rat that is on top that is more likely to emit 50-kHz USVs. These findings suggest that, for juveniles, 50-kHz USVs may have a critical function in maintaining and facilitating playful motivation, but a more limited role in signaling playful actions. In adults, however, whatever the motivational role of such calling may be, the various kinds of USVs appear to serve critical communicatory functions. For instance, when pairs of adult males that are unfamiliar with one another encounter each other in a neutral arena, they play together, but if one partner is devocalized, there is a significantly higher likelihood that the interaction will escalate to become aggressive. While the relative roles of appetitive 50-kHz and aversive 22-kHz USVs in this context remain to be determined, our overall findings for play in both juveniles and adults suggest that 50-kHz USVs likely have multiple functions, with different functions being more prevalent at some ages and contexts than others.

Rough-and-tumble play (RT) is a widespread phenomenon in mammals. Since it involves competition, whereby one animal attempts to gain advantage over another, RT runs the risk of escalation to serious fighting. Competition is typically curtailed by some degree of cooperation and different signals help negotiate potential mishaps during RT. This review provides a framework for such signals, showing that they range along two dimensions: one from signals borrowed from other functional contexts to those that are unique to play, and the other from purely emotional expressions to highly cognitive (intentional) constructions. Some animal taxa have exaggerated the emotional and cognitive interplay aspects of play signals, yielding admixtures of communication that have led to complex forms of RT. This complexity has been further exaggerated in some lineages by the development of specific novel gestures that can be used to negotiate playful mood and entice reluctant partners. Play-derived gestures may provide new mechanisms by which more sophisticated communication forms can evolve. Therefore, RT and playful communication provide a window into the study of social cognition, emotional regulation and the evolution of communication systems., (© 2015 Cambridge Philosophical Society.)

Autism is a severe neurodevelopmental disorder characterized by qualitative impairments in social behavior, communication, and aberrant repetitive behaviors. A major focus of animal models of autism has been to mimic the social deficits of the disorder. The present study assessed whether rats exposed prenatally to valproic acid (VPA) show deficits in social play as juveniles that are consistent with the social deficits observed in autism. Dams were exposed to an acute dose of VPA on gestational day 12.5. Later, the playful interactions and associated ultrasonic vocalizations of the juveniles were examined. It was predicted that VPA-treated rats should play less than the controls. Characteristic of neurobehavioral insult at this early age, the VPA-treated juveniles showed significant increases in the frequency of body shakes and sexual mounting, but played at the same frequency as the controls. However, when playing, they were less likely to use tactics that facilitated bodily contact and vocalized less. These data suggest that prenatal VPA exposure disrupts some aspects of being able to communicate effectively and engage partners in dynamic interactions - deficits that are consistent with those observed in autism.

When playing, rats emit 50-kHz calls which may function as play signals. A previous study using devocalized rats provides support for the hypothesis that 50-kHz function to promote and maintain playful interactions (Kisko et al., 2015). However, in that study, all pairs were cage mates and familiar with each other's playful tendencies that could have attenuated the role of play signals. The present study uses unfamiliar pairs to eliminate any chance for such attenuation. Four hypotheses about how 50-kHz calls could act as play signals were tested, that (1) they maintain the playful mood of the partner, (2) they are used to locate partners, (3) they attract play partners and (4) they reduce the risk of playful encounters from escalating to serious fights. Predictions arising from the first three hypotheses, tested in juveniles, were not supported, suggesting that, for juveniles, 50-kHz calls are not facilitating playful interactions as play signals. The fourth hypothesis, however, was supported in adults, but not in juveniles, in that unfamiliar adult males were more likely to escalate playful encounters into serious fights when one partner was devocalized. These findings suggest that vocalizations at most have a minor role in juvenile play but serve a more central role in modulating adult interactions between strangers, allowing for the tactical mitigation of the risk of aggression., (Copyright © 2015 Elsevier B.V. All rights reserved.)

During competitive interactions, such as fighting and predation, animals perform various actions, some of which are easy to characterize and label, some of which are reliably repeated. Such 'behavior patterns' are often the measures of choice when comparing across species and experimental contexts. However, as Bob Blanchard and others have pointed out, such measurements can be misleading as in competitive interactions in which the animals compete for some advantage, often the biting or otherwise contacting a particular target on the opponent's body. In this context, the animals' behavior is better analyzed in terms of the tactics of attack and defense deployed by the combatants to gain or avoid contact with those targets. Several examples are shown to reveal that this is an important distinction as simply scoring predefined behavior patterns can obscure the dynamic context in which the actions are performed. This can lead to confounding species and experimental differences and the mislabeling of combat actions as communicatory signals., (Copyright © 2015. Published by Elsevier Inc.)

During playful interactions, juvenile rats emit many 50-kHz ultrasonic vocalizations, which are associated with a positive affective state. In addition, these calls may also serve a communicative role - as play signals that promote playful contact. Consistent with this hypothesis, a previous study found that vocalizations are more frequent prior to playful contact than after contact is terminated. The present study uses devocalized rats to test three predictions arising from the play signals hypothesis. First, if vocalizations are used to facilitate contact, then in pairs of rats in which one is devocalized, the higher frequency of pre-contact calling should only be present when the intact rat is initiating the approach. Second, when both partners in a playing pair are devocalized, the frequency of play should be reduced and the typical pattern of playful wrestling disrupted. Finally, when given a choice to play with a vocal and a non-vocal partner, rats should prefer to play with the one able to vocalize. The second prediction was supported in that the frequency of playful interactions as well as some typical patterns of play was disrupted. Even though the data for the other two predictions did not produce the expected findings, they support the conclusion that, in rats, 50-kHz calls are likely to function to maintain a playful mood and for them to signal to one another during play fighting., (Copyright © 2014 Elsevier B.V. All rights reserved.)

Alterations in social behavior are among the major negative consequences observed in children with Fetal Alcohol Spectrum Disorders (FASDs). Several independent laboratories have demonstrated robust alterations in the social behavior of rodents exposed to alcohol during brain development across a wide range of exposure durations, timing, doses, and ages at the time of behavioral quantification. Prior work from this laboratory has identified reliable alterations in specific forms of social interaction following moderate prenatal alcohol exposure (PAE) in the rat that persist well into adulthood, including increased wrestling and decreased investigation. These behavioral alterations have been useful in identifying neural circuits altered by moderate PAE(1), and may hold importance for progressing toward a more complete understanding of the neural bases of PAE-related alterations in social behavior. This paper describes procedures for performing moderate PAE in which rat dams voluntarily consume ethanol or saccharin (control) throughout gestation, and measurement of social behaviors in adult offspring.

Rats with juvenile play experience display a greater ability in coordinating their movements with social partners than those deprived of such experience, and this may be due to the play-induced neural restructuring of the medial prefrontal cortex (mPFC). The present study investigates the role of the mPFC in interanimal coordination. Rats with and without bilateral mPFC lesions were tested on a robbing-and-dodging task. This food protection task measures the ability of rats to protect pieces of food by gaining and maintaining an interanimal distance between themselves and the rat attempting to rob the food. Given that mPFC lesions have been associated with sensory and motor deficits, the same rats were also subjected to a task to measure skilled motor movements. Rats with bilateral mPFC lesions had more food stolen and displayed an inability to maintain interanimal distance with partner, but did not exhibit any motor or sensory deficits. These findings suggest that the mPFC is involved in interanimal coordination and that the play-induced neural restructuring of this area may account for the enhanced coordination seen in rats with prior play experience., (PsycINFO Database Record (c) 2014 APA, all rights reserved.)

Laboratory strains of rats are a commonly used subject to study play behavior. Recent research has shown that play in one laboratory strain of rat (e.g., Long-Evans hooded) differs in a number of ways from its wild counterparts. These findings suggest that domestication affects some aspects of play behavior. However, there are multiple strains of laboratory rats, which have been domesticated through different lineages all derived from wild rats and it cannot be assumed that all domestic strains are identical in their play. Therefore, the aim of this study was to compare the play behavior of three other strains of laboratory rats (e.g., Wistar, Sprague-Dawley, and Brown Norway). All strains were similar to each other as they all engaged in high frequencies of play, tolerated similar interanimal distances before initiating playful defense and displayed similar acrobatic capacities, suggesting domestication produces some common changes in play and other factors that influence play. However, strains differed significantly from one another in the use of tactics that promote bodily contact during play. Indeed, in this regard, some strains were more similar to wild rats than others, suggesting that some domestication-induced changes are either unique or more prominent in some laboratory strains than others. Such a mosaic pattern of transformation not only offers the possibility of using strain differences to characterize the genetic factors contributing to different facets of play, but also cautions researchers from making rat-general conclusions from studies on any one strain.

Juvenile play experiences promote behavioral flexibility in rats. If other early positive experiences, such as tactile stimulation, are given prior to exposure to psychostimulants, the behavioral response to the drug is attenuated. The objective of the present study was to determine if the experience of juvenile play behavior would attenuate the response to nicotine. Two experiments were conducted: (1) behavioral sensitization to nicotine exposure, and (2) voluntary consumption of nicotine. For both experiments, rats were reared either with three same-sex peers (play group) or one adult (no play group) during their juvenile period. Then, as adults, half of each group was exposed to repeated injections of nicotine and the other half to saline. Prior play experience had no effect on behavioral sensitization or on voluntary consumption of nicotine. It remains to be determined whether juvenile experience with play influences the rewarding properties of nicotine in social contexts as adults., (© 2013 Wiley Periodicals, Inc.)

During playful interactions, rats emit increased levels of 50-kHz vocalizations. It is possible that these vocalizations are used as play signals that promote and maintain playful contact. The study investigated this possibility. It was predicted that if these vocalizations are used as play signals, they should be more prevalent (1) before an attack, (2) in attacks leading to wrestling, and (3) in males compared to females, as males play more roughly. Moreover, given that there are at least 15 different subtypes of 50-kHz calls, it is possible that different calls are used in different contexts. Therefore, our prediction (4) was that different subtypes would be used for initiating and terminating playful contact. Pairs of same-sex juveniles were tested so that video recordings of their play and audio recordings of their vocalizations were synchronized. 50-kHz vocalizations occur more often before an attack and in male pairs. Specific calls were associated with specific types of behaviors and these associations differed between male and female rats. However, calls were not more frequent in attacks leading to wrestling than in attacks leading to withdrawal. The data provide qualified support for the hypothesis that 50-kHz vocalizations function as play signals., (Copyright © 2014 Elsevier B.V. All rights reserved.)

Juvenile play behavior in rats promotes later behavioral flexibility and appears to do so by modifying the neural systems that regulate the animal's response to unexpected challenges. For example, the experience of play has been shown to prune the dendritic arbor of the cells in the medial prefrontal cortex (mPFC), part of the brain's executive control system. The objective of the present study was to determine if the play-induced changes in the mPFC promotes greater plasticity to experiences later in life. In order to test this possibility, exposure to nicotine was used as the secondary experience given later in life, as it has been shown to produce later changes to the morphology of mPFC pyramidal neurons. Animals were either paired with three same-sex peers (play condition) or one adult (no play condition) during their juvenile period. As young adults, half of the rats from each condition were exposed to repeated injections of nicotine and the other half to injections of saline. The neural plasticity of the mPFC was measured by changes in length and branching of dendrites. Neural changes induced separately by play and by nicotine were consistent with previously published findings. The novel finding was that the cells in the mPFC exhibit a greater response to exposure to nicotine if the rats first had play experience. These findings suggest that juvenile play experiences enhance the plasticity of some neural systems., (Copyright © 2013 Elsevier Ireland Ltd. All rights reserved.)

Laboratory rats have been widely used to study the development and neural underpinnings of play behavior. However, it is not known whether domestic rats play in the same way and at the same frequency as their wild counterparts. In this study, the play of juvenile rats from a colony of wild rats maintained in captivity was compared to that of a strain of domesticated rats (e.g., Long Evans hooded). Three predictions were tested. First, it was predicted that wild rats would incorporate more agonistic behavior in their play. This was not found, as in all cases, both the wild and the laboratory rats attacked and defended the nape during play, a nonagonistic body target. Second, because play is typically more frequent in domesticated animals than their wild progenitors, it was predicted that the wild rats should play less than the laboratory rats. This was found to be the case. Third, because wild animals tend to be less tolerant of proximity by conspecifics and tend to be more agile in their movements, it was predicted that there would be less contact between wild pair mates. This was found to be the case; data show that the play of laboratory rats involves the same target (i.e., the nape of the neck) and tactics of defense as those used by wild rats. However, the laboratory rats initiated playful attacks more frequently, and were more likely to use tactics that promoted bodily contact. These similarities and differences need to be considered when using laboratory animals as models for play in general.

Play fighting in the rat involves attack and defense of the nape of the neck, which if contacted, is gently nuzzled with the snout. Because the movements of one animal are countered by the actions of its partner, play fighting is a complex, dynamic interaction. This dynamic complexity raises methodological problems about what to score for experimental studies. We present a scoring schema that is sensitive to the correlated nature of the actions performed. The frequency of play fighting can be measured by counting the number of playful nape attacks occurring per unit time. However, playful defense, as it can only occur in response to attack, is necessarily a contingent measure that is best measured as a percentage (#attacks defended/total # attacks X 100%). How a particular attack is defended against can involve one of several tactics, and these are contingent on defense having taken place; consequently, the type of defense is also best expressed contingently as a percentage. Two experiments illustrate how these measurements can be used to detect the effect of brain damage on play fighting even when there is no effect on overall playfulness. That is, the schema presented here is designed to detect and evaluate changes in the content of play following an experimental treatment.

We examined whether people with Parkinson disease (PD) have difficulty negotiating a gait obstruction in threatening (gait path and obstacle raised above floor) and nonthreatening (gait path and obstacle at floor level) contexts. Ten PD patients were tested in both Meds OFF and Meds ON states, along with 10 age-matched controls. Participants completed 18 gait trials, walking 4.7 m at a self-selected speed while attempting to cross an obstacle 0.15 m in height placed near the centre point of the walkway. Kinematic and kinetic parameters were measured, and obstacle contact errors were tallied. Results indicated that PD patients made more obstacle contacts than control participants in the threatening context. Successful crossings by PD patients in the threatening condition also exhibited kinematic differences, with Meds OFF PD patients making shorter crossing steps, with decreased initiation and crossing velocities. The findings from this study lend support to the theory that PD patients rely on directed attention to initiate and control movement, while providing indication that the motor improvements provided by current PD pharmacotherapy may be limited by contextual interference. These movement patterns may be placing PD patients at risk of obstacle contact and falling.

Aye-ayes (Daubentonia madagascerensis) have highly specialized hands with long digits, especially the thin middle one (D3), which is used for extracting food, such as beetle larvae, under bark. Due to the elongation of their fingers, including the thumb, it is presumed that aye-ayes have a rather limited capacity for delicate manipulation of objects. However, studies have reported independent movement of digits D3 and D4, and one report noted a seemingly independent thumb (D1) movement in holding food. Sixteen captive adult aye-ayes were videotaped feeding on a diverse range of foods so as to document how the thumb is used during food holding. To determine if the patterns observed were unique to aye-ayes, 24 individuals from 9 other species of lemurs were also videotaped. Two patterns of thumb use idiosyncratic to aye-ayes and one other lemur, the sifaka (Propithecus verreauxi), were identified: (1) when holding a food item in one hand, the thumb was used to secure the food, with the other digits playing a secondary role; (2) when holding a food item with both hands, the thumbs once again took a predominant role in securing the food. In the majority of these cases, whether held by one or two thumbs, the thumbs curled around the item, but some descriptive evidence is provided that suggests that aye-ayes exaggerate the role of the thumbs by shifting the hold to the outer edge. The novel uses of the thumbs in aye-ayes demonstrate that brain mechanisms can sometimes override the behavioral (or motor) limitations imposed by the morphology of the body., (Copyright © 2011 Elsevier B.V. All rights reserved.)