Play fighting and the development of the social brain: The rat's tale.

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.

Is play a behavior system, and, if so, what kind?

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.

"I am going to groom you": Multiple forms of play fighting in gray mouse lemurs (Microcebus murinus).

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

What is play fighting and what is it good for?

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.

From Play to Aggression: High-Frequency 50-kHz Ultrasonic Vocalizations as Play and Appeasement Signals in Rats.

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.

Peering into the dynamics of social interactions: measuring play fighting in rats.

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.

Anatomy is important, but need not be destiny: novel uses of the thumb in aye-ayes compared to other lemurs.

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.

The use of the bared-teeth display during play fighting in Tonkean macaques (Macaca tonkeana): sometimes it is all about oneself.

Play signals are viewed as important means by which animals inform each other that bites, strikes, and throws that occur during play fighting are indeed playful rather than serious. One such signal is the open mouth play face that is common in primates and many other mammals. Unfortunately, as most play fighting involves biting, it can be ambiguous as to whether any instance of opening the mouth is performed to communicate playful intent or is simply a preparation for biting. In this study, open mouths co-occurring with the bared-teeth display (teeth-baring) in Tonkean macaques were used to assess the context in which facial gestures only relevant for signaling (i.e., teeth-baring is not necessary for biting) are used during play. Two predictions arising from the hypothesis that play signals are used to facilitate playful contact were tested: that the open mouth with teeth-baring should (1) be most frequent preceding contact, and (2) that it should be performed most often when bites are directed at orientations that is visible to the recipient. The data only partially support these predictions. The open mouth with teeth-baring is also frequently used when a monkey withdraws from playful contact. Moreover, it is associated with bites to body targets, such as the rump, that offer little prospect for detection by the recipient; this supports the possibility that play signals may sometimes be emitted not to communicate with the partner but with the performer itself. Thus, play signals serve multiple functions during play fighting.

To whom the play signal is directed: a study of headshaking in black-handed spider monkeys (Ateles geoffroyi).

Spider monkeys shake their heads so as to facilitate amicable social contact. This occurs frequently during vigorous play fighting, and so is common during the juvenile period. Occasionally, juvenile spider monkeys use headshakes during nonsocial locomotor play. In this study, head shaking in early infancy and in adulthood was studied in a captive troop of spider monkeys, with a total of 8 infants studied from shortly after birth to just before weaning. Three hypotheses to account for these nonsocial headshakes were tested. The play as the experience of the unexpected hypothesis was found wanting because nonsocial headshakes were most common in early infancy, before the onset of the juvenile peak in play. The immature misdirection of signals hypothesis was also found wanting because the headshakes were correctly directed at other monkeys, but not at inanimate objects that were grabbed and mouthed. Both also failed to predict the occurrence of the observed nonsocial headshakes in adults. The hypothesis best supported by the data is that, under some situations, headshakes are self-directed to promote action when confronting contexts of uncertainty.