Rough and Tumble Play

• Dr. Vivien Pellis, University of Lethbridge, Lethbridge, Alberta, Canada

• Dr. Sergio Pellis, University of Lethbridge, Lethbridge, Alberta, Canada

Figure 1: Two juvenile male rats are shown, at about 35 days old, engaging in a play fight in which they compete for access to the napes of each other’s necks. One rat approaches from behind towards the nape of the partner’s neck (a, b). The partner then defends by turning to face (c, d), but is knocked over on to its back (e-g). The rats struggle to gain access at each other’s napes as the original attacker stands over the supine partner (i-l), until the rat on the bottom pushes the partner off (m, n) and then launches its own attack to the nape from the rear (o) (From Pellis & Pellis (1987), copyright 1987 by Wiley. Copied with permission.

Rough-and-tumble play, also called play fighting, is a form of play in which partners compete with one another to gain some advantage (e.g., strike, bite, push onto ground), but do so without the severity or consequences of serious fighting, which it resembles (Aldis, 1975). Play fighting is one of the most commonly reported forms of play (Pellis & Pellis, 1998), having some basic commonalities across most species that play, including humans (Pellis et al., 2010a). These include the insertion of co-operative behavior into sequences of playful competition that make play fighting reciprocal and so ‘fair’ (Bekoff, 2001). Given this prevalence and similarity across a wide swathe of species, most notably in birds and mammals, but also possibly in other vertebrate (e.g., some reptiles and fish) and invertebrate (e.g., some insects) lineages (Burghardt, 2005), play fighting is ideally suited for studying the brain mechanisms by which play is produced and how it has evolved (Pellis & Pellis, 2009). Although there are many studies of play fighting in a diverse range of species (Burghardt, 2005; Fagen, 1981), the most intensively studied species is the rat, especially its domesticated version suitable for laboratory research, and the knowledge gained from this model species has implications for our understanding of play in general (Pellis & Pellis, 2009).

Play fighting in rats involves attack and defense of the nape of the neck, which if contacted is nuzzled with the snout (Figure 1). The body target and what is done to that body target in the play of rats is revealing in two important ways. First, it is not a simulation of what occurs during serious fighting, in which the rump is attacked and bitten, but a simulation of courtship behavior, in which the male rat nuzzles the female’s nape prior to mounting. Comparison of rats with other rodents and more widely to other mammals, shows that play fighting can be derived from competition of sexual targets as well as targets attacked during serious fighting and in predatory behavior (Pellis & Pellis, 2009). However, irrespective of whether play fighting is derived from aggressive, sexual or predatory behavior, it follows the same rules: that ensure it is reciprocal, with partners alternating roles of attack and defense (Pellis et al., 2010a). Second, an important feature of play fighting is that even though the advantage can be achieved in many different ways – with the hands in humans, with the snout in rats and with the mouth in dogs – bodily contact is essential to provide the pleasure and reward that arises from engaging in this behavior (Panksepp & Burgdorf, 2003). It is the pleasure derived from contacting the partner that motivates play fighting and it is the pleasure gained by the partner through such contact that provides a means of manipulating the affective state of partners (Pellis & Pellis, 2010). These two properties, reciprocity and tactile contact, lay the foundations for two important functions of play fighting.

Play fighting as a tool for the development of the social brain

As is the case across many species, play fighting in rats is most common in the juvenile period, and an enduring question has been regarding the benefits that may accrue from playing at this age (Fagen, 1981). Rats have provided considerable insight into this question. Many laboratories have shown that the absence of peer-peer interactions in the juvenile period leads to a variety of deficits in cognitive, social and emotional skills. Studies from the 1960s and 1970s mostly produced these effects by rearing juveniles in isolation, but, of course, this creates a highly stressful environment – for most social animals, living in social isolation is disturbing, as evidenced by social isolation being a form of human punishment in prison. Furthermore, complete isolation denies the young rat of many social experiences, not just play. From the late 1970s onwards, a series of ingenuous methods were developed specifically to deprive young rats of social play experience while retaining other social experiences and these consistently showed that, in the absence of play fighting experience as juveniles, adult rats have social and emotional deficits (Pellis & Pellis, 2006). Two questions arise from these findings: What is it about play that improves social and emotional skills and how do these play-induced changes alter adult skills? Recent work on rats has begun to reveal answers to these questions.

Figure 2: During play fighting, rats often adopt a posture in which one animal is standing over another that is lying on its back. When standing on top, rats typically do so with their hind paws on the ground, this provides it with postural support and so frees its forepaws in order to hold and restrain its partner (a). However, sometimes, and especially in the juvenile period, the rat on top stands with all four paws on its supine partner (b). This position is unstable, as the supine partner is usually squirming underneath it. (From Foroud & Pellis (2003), copyright 2003 by Wiley. Copied with permission).

Play and the experience of the unexpected: While play may occur before and after the juvenile period, it is generally most frequent in juveniles, and, for some species, like the rat, it is also qualitatively different. The rules that promote reciprocity are exaggerated, which leads to more frequent role reversals (Pellis et al., 2005). This is achieved by the juvenile rats performing actions that make it difficult for them to keep their postural stability and so control either their own or their partner’s behavior. For example, when one rat defends its nape by rolling over onto its back, the partner stands over it using its forepaws to restrain the movements of the supine animal, with its postural stability ensured by keeping its hind feet firmly planted on the ground (Figure 2a). However, in the juvenile period, rats are more likely to circumvent this stable postural configuration by standing on their squirming, supine partner with all four feet (Figure 2b). When a rat is standing on top of its partner with its hind feet anchored on the ground, counterattacks by its once supine partner are only likely to lead to role reversals 30% of the time, but when standing on the supine partner with all four feet, the chance of a reversal jumps to 70% (Pellis et al., 2005). Thus, during the juvenile period, rats perform actions that increase their experience of unpredictability, and such behavior is consistent with the theory that one of the functions of juvenile play experience is to train for the unexpected (Spinka et al., 2001). Data from various laboratories and studies on various species are generally consistent with this view (Pellis & Pellis, 2006). So, one way that play could influence the development of social skills and the emotional regulation to execute those skills properly, is for play to provide a relatively safe milieu within which to experience loss of control and not to be overly emotionally distraught when this occurs (Pellis & Pellis, 2009).

The role of play in shaping the social and emotional brain: In the absence of play experience, animals typically develop their species-typical behavioral repertoire normally (Martin & Caro, 1985), suggesting that play is not necessary for developing the brain mechanisms that produce behavior. Indeed, with the cortex removed - the largest and most recently evolved part of the brain - rats can still perform all the behavior patterns typical of play and do so at a frequency typical of intact rats. However, as already mentioned, when confronting novel, unexpected, or otherwise disturbing situations, rats that have not had play experience as juveniles are less able to cope, and this is reflected by them not using the appropriate behavior patterns. Similarly, rats with the cortex removed can function seemingly normally in a stable environment, such as their home cage, but when confronted by novelty, are unable to adapt (Kolb & Whishaw, 2008). With regard to the particular deficits exhibited by rats that did not play as juveniles, damage to the prefrontal cortex (PFC), the area of the cortex most critical to executive function which involves selecting appropriate actions or inhibiting inappropriate ones, produces adult rats that have similar social deficits. Therefore, it is likely that the beneficial effects of play experience in the juvenile period is to modify the development of the PFC, giving it greater control over the brain circuits, lower in the brain, that generate behavior patterns and regulate emotions. Indeed, play experience in the juvenile period has been shown to change the anatomical properties of the neurons of the PFC (Pellis et al., 2010b).

The neurons of different parts of the PFC appear to be more or less sensitive to the modifying effects of different social experiences during the juvenile period, but what is clear is that, one sub-region of the PFC, the medial prefrontal cortex (mPFC), is strongly influenced by the experience of play. The mPFC has strong connections to brain areas that regulate emotions and that select appropriate behavior patterns for particular tasks (Pellis & Pellis, 2011). These findings in rats indicate that the unique features of play fighting in the juvenile period - the exaggerated experience of unpredictable loss of control – modify the executive function capabilities of the mPFC, and this produces adults that are more able to deal with the vicissitudes of life. Such improvement may be due to being better able to select the most appropriate actions given the circumstance or by inhibiting an emotional over reaction to an unexpected situation, or to some combination of the two.

Play as a tool for social assessment and manipulation

Some species, including humans and many other primates, continue to play as adults, and at this stage of the life cycle, rather than functioning to promote the future development of the brain, it functions to serve immediate purposes, such as calming social discord, reducing stress and testing out relationships within a social group or with strangers (Palagi, 2011). It is likely, that the physical touching that is central to play fighting is an important vehicle through which such manipulation occurs, as social touching is important for inducing the release of neurochemicals that facilitate social cooperation (Pellis & Pellis, 2010). Rats, unlike many other species of rodents, also retain play fighting in adulthood and use it for assessment and manipulation of dominance relationships (Pellis, 2002), and again, rats have provided some insights into the uses of play in adulthood.

Rats live in large colonies composed of many males, many females and their offspring, with males dominant over females and one of the males being dominant over the others. In this milieu, the dominant rat has priority of access to food and sexually receptive females. This leaves the subordinate males with two options: stay and pick up the scraps left by the dominant, or try to usurp the dominant role either in the home colony or in a new one. Play fighting among adult male rats is mostly used by the subordinate males who use it to either re-affirm their subordinate status with the dominant or to test the dominant or an unfamiliar male for changes in dominance status. When playing with another subordinate or a female, a subordinate male does so using the rougher, adult male typical pattern, but when playing with a dominant male, reverts to the gentler, juvenile typical pattern of play. Furthermore, when given the choice, females and subordinate males are more likely to groom and play with the dominant than with each other. By seeking out the dominant with which to play and by doing so using the gentler pattern of play, the subordinates are reminding the dominant that they belong to the colony and that they acknowledge him as the dominant animal. However, a subordinate may also use play fighting to test whether the status of the dominant animal can be reversed. This is done by incrementally increasing the roughness of the play, and if the dominant backs down, then their relative status can be reversed. But if the dominant responds by increasing its own roughness, then the subordinate can back down by stopping its play or reducing its roughness (Pellis, 2002).

In rats, the use of adult play fighting seems to be limited to these dominance related contexts, but in other species, as indicated above, such play can be used in a wide variety of social contexts to test and probe social relationships (Palagi, 2011; Pellis & Pellis, 2009).

A Caveat

While rats have been useful in delineating the ways in which play fighting can be used to both sharpen social skills during juvenile development and as a tool for social assessment and manipulation at later ages, it is important to note that these findings have been made on domesticated rats. In captivity, rats are typically maintained at lower densities than is case for their free-living, wild cousins, and have, like other domesticated animals (Coppinger & Coppinger, 2001), been selectively bred for tameness. That is, after 100 years of domestication, laboratory rats have been adapted for a life that differs markedly from that of their wild ancestors. Consequently, the functional properties of play in laboratory rats may be a product of the domestication process. However, wild rats have been reported to play as juveniles and even adult-adult playful interactions of the kind described above have been reported (see references to this early literature in Smith et al., 1999). So, it is possible that the pattern seen in laboratory rats is an embellishment of that seen in the wild, although this remains to be empirically determined. Even if the functional patterns seen in the play of laboratory rats are a product of domestication, understanding these functional roles, and the mechanisms that regulate them, would still provide a useful model for study in other species, including wild rats, as these pinpoint the features of play that make such functions possible (see below).

Why is play fighting suited to these delayed and immediate functions?

As noted above, for play fighting to remain playful, there has to be an element of cooperation as well as competition, permitting the encounter to be reciprocal. But of course, in the exuberance of the moment, one partner may push, hit or bite harder than expected, and then the problem faced by the recipient is to decide whether it was an unintended mistake or a deliberate transgression of the rules. And then there is the problem of repeat offenders. Indeed, in both humans and other animals, cases have been reported in which a partner persistently lacks restraint in their play and potential play partners ostracize them, refusing to engage them in play (Suomi, 2005; Wilmer, 1991). That is, play fighting has an element of ambiguity in its organization, and both the role of play fighting in training the executive function of the PFC in the juvenile period and of using play fighting to negotiate social relationships in adulthood seems to depend on this property of play fighting.

During the juvenile period, when the PFC is maturing, the unpredictability created by the ambiguity in play fighting provides a venue for the PFC to practice its executive functions. That is, it forces the PFC to work to decide whether a particular transgression during play fighting should be treated as serious, and if so, what to do about it. In 4-6 year old children, giving them playful experiences involving some form of cooperation with a partner, has been shown to improve executive function (Diamond et al., 2007). For example, when two children are asked to jointly construct a drawing, they have to make a number of decisions that involve negotiation – what to draw, who draws which components, who goes first, and so on. In play fighting, such decisions are called for, but in a much more dynamic and unpredictable context. Not surprising, then, that such play experience both modifies the anatomy of the PFC and improves social skills and emotional regulation (Pellis et al., 2010b).

In adulthood, testing relationships can be dangerous, as a subordinate initiating play that is too rough with a dominant can lead to serious retaliation, as can physically contacting an unfamiliar animal. However, play can provide a platform for such testing because there is an element of ambiguity, in which deviating just a little from the rules that ensure reciprocity can be done relatively safely. If the recipient of the rough play reacts by tensing or otherwise indicating aggression, the initiator can back down and revert back to gentler play. Indeed, some species have a rich repertoire of play signals, and in such species, such signals can be used to inform the partner that the actions that have preceded, and are considered offensive by the partner, are not to be taken seriously, as they were ‘just play’ (Aldis, 1975). That is, because of the inherent ambiguity in play fighting, such play can be used to test and probe relationships in a way that more forthright behavioral approaches (e.g., directly challenging the dominance of a partner), cannot (Pellis & Pellis, 2009).

References

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Sponsored by: Megan Tulac, National Institute for Play, Carmel Valley, CA, USA

Reviewed by: Dr. Gordon M. Burghardt, University of Tennessee, Knoxville, Knoxville, TN, USA

Reviewed by: Megan Tulac, National Institute for Play, Carmel Valley, CA, USA

Accepted on: 2012-11-10 17:56:08 GMT