Rough-and-Tumble Play and the Development of the Social Brain

By Sergio M. Pellis and Vivien C. Pellis

Submitted by Carlie Ramotowski, Lethbridge School Division

In the schoolyard, Johnny sneaks up behind Freddy, grabs him by the shoulders, and flings him to the ground. Johnny prances around smiling and laughing while Freddy regains his composure. Freddy then smiles at Johnny, and the two run off together.

Such rough-and-tumble play may seem frivolous or even dangerous, and as a consequence, many schools have worked toward eliminating it (Bjorklund & Pellegrini, 2002). However, rough-and-tumble play is a recurring feature of childhood, and several studies show that engagement in such play is correlated with measures of social competence (Pellegrini, 1995).

Of course, it is not possible to do the critical experiments with human subjects to determine whether there is a causal link between play and social competence. Experimental work from many laboratories using nonhuman animals, especially rats, suggests such a causal link, and researchers are beginning to characterize the possible mechanisms involved.

Understanding Play Fighting

In nonhuman animals, rough-and-tumble play, also known as play fighting, is one of the forms of play most often reported by researchers (Pellis & Pellis, 1998), and, certainly within the laboratory context, it is the most intensively studied (Panksepp, 1998).

As is true for play in general, there is no accepted definition of play fighting, but there is growing agreement about some of its key elements (Burghardt, 2005), such as being engaged in voluntarily and being associated with positive affect.

Nonetheless, because play fighting varies in degree of roughness, there is still debate about when it becomes serious fighting. Fortunately, in rats there is a clear behavioral difference between play fighting and serious fighting.

During play fighting, rats compete for access to the nape of their partner’s neck, which if contacted is nuzzled. In serious fighting, they compete for access to the rump and the lower flanks of their partner’s body, which if contacted are bitten (Pellis & Pellis, 1987).

Thus, even though the rats appear to be competing and often vary in the degree of roughness, the targeting of the nape makes play fights readily discernible from serious fights.

Play fighting involves playful attack by one partner coupled with playful defense by the other, with the role of attacker and defender alternating. The ease with which such roles alternate depends on attack and defense tactics; there is considerable independence between the frequency of attack and the types of defense tactics used.

Such independence has provided a fertile resource for linking different features of play fighting to different neural mechanisms (Pellis & Pellis, 1998). These neural mechanisms suggest a means by which play fighting may influence the development of social competency.

The Benefits of Play

Adult rats that have been prevented from playing with peers as juveniles have many emotional and cognitive deficits. Among the most striking of these are social problems such as hyper-defensiveness to the approach of another rat and difficulty in coordinating movements with those of a social partner—either in a cooperative encounter such as sex or in a competitive encounter such as defending a piece of food (for a review, see Pellis & Pellis, 2006).

Studies by a Dutch group (see, e.g., von Frijtag, Schot, van den Bos, & Spruijt, 2002) capitalized on the social organization of rats, which involves multimale and multi-female colonies within which one adult male assumes the dominant role.

Under natural conditions, younger males may intrude into the territory of a colony, seeking to establish residency. The dominant male of a colony typically resists such intrusions by attacking the unfamiliar males.

After establishing such colonies in a laboratory, groups of young adult males were introduced into the colonies. Some of these males had been reared together and so had plenty of opportunity to play fight, and some had been reared in isolation, with no play-fighting opportunities.

When introduced into a colony, the rats that had been reared with peers quickly learned that if they remained crouched and motionless, attacks from the dominant male diminished. Similarly, when placed in a colony that contained a platform on which the rats could perch and so avoid contact with the dominant, the rats that were reared socially quickly learned to move onto and remain on the platform.

In contrast, the play-deprived rats did not learn that remaining motionless would reduce attention from the dominant; they continued to move about the cage and so attracted further serious attacks. Furthermore, the play-deprived rats failed to take advantage of the platform as refuge.

The play-deprived rats also produced higher levels of stress hormones and maintained these levels for longer periods of time than the rats raised with peers (e.g., von Frijtag et al., 2002), thus exposing them to the detrimental effects of chronic stress.

The picture that emerges is one in which play-deprived rats are overly stressed by novel social encounters and are poor at adopting strategies that can alleviate that stress. Thus, it appears that in rats, the opportunity to engage in play fighting as juveniles is critical for the development not only of cognitive and emotional competency but also social competency.

However, there is an important caveat to consider.

When rats are deprived of play fighting, they are usually deprived of other forms of social contact as well, and so the contributions from non-playful social contact cannot be discounted.

Nonetheless, a large body of evidence strongly suggests that although a role for non-playful social contact cannot be discounted, the experience of peer–peer play fighting is crucial (for a review, see Pellis & Pellis, 2006).

In a particularly illuminating series of studies, Dorothy Einon and her colleagues (e.g., Einon & Morgan, 1977) showed that rats that were reared as pairs but with mesh partitions between them so that they could see, smell, and lean against each other, still had cognitive and social deficiencies as adults.

Further, rats that were reared in the same cage with an adult, a situation that provides the opportunity for direct social contact but little opportunity to engage in play fighting, also showed such deficiencies as adults.

Rats reared in isolation but given access to an age-matched partner for 1 hour per day throughout the juvenile period performed as well as controls did in a number of cognitive tests as adults. For most of that hour, the young rats engaged in play fighting.

Not coincidentally, rats reared with a litter of siblings play for about an hour a day. The experience of play fighting during the juvenile period seems to be a crucial ingredient for normal development.

Why the Juvenile Period Matters

Our own research on rats has shown that play fighting has specific properties in the juvenile phase and that these properties may provide a clue to how the behavior contributes to normal development.

In rats, play fighting first occurs just before weaning, around the 3rd week after birth; it peaks between 30 and 40 days of age, and declines around puberty, the 8th to 9th week.

When we examined the content of the play, we found that when play fighting is at its peak, it has a juvenile-typical quality—that is, offensive and defensive tactics are organized to decrease the control that the rats have on their own and their partners’ movements.

This organization results in more frequent role reversals and provides the juvenile rats with an increased opportunity to experience not only novel bodily movements but also continually changing bodily configurations with their partners.

The play fighting that occurs before this peak period more closely resembles that of postpubescent animals, which is far more stereotyped in the organization of the movements involved; thus the pattern of play in the juvenile phase is unique (for a review, see Pellis, Pellis, & Foroud, 2005).

But what is it about the unique pattern of play fighting in the juvenile period that provides the experiences that promote normal development?

Rats reared in isolation can perform all socially relevant behavior patterns, but because their ability to coordinate their movements appropriately with those of their opponents is impaired, they may fail to orient their bodies correctly relative to the position of their opponents (e.g., Pellis, Field, & Whishaw, 1999).

This apparent lack of ability to calibrate movements with those of a partner is a significant deficit in juvenile rats deprived of play fighting.

Furthermore, such insensitivity to the outside world may also lay the foundation for the failure to develop emotional and cognitive skills in general. Indeed, there is growing evidence for a connection between the development of movement and the development of cognition (e.g., Diamond, 2000).

Like all complex behaviors, play fighting involves many areas of the brain.

The behavior patterns are likely organized in the lower brainstem; the motivation to engage in such behavior is organized in the mid-brain and the lower forebrain, which encompasses the reward systems of the brain; and finally, the cortex fine-tunes play fighting so that it is modified appropriately with context and past experience (Panksepp, 1998).

Because play fighting is a highly social activity, when rats play fight, those areas of the brain that work together to deal with social phenomena—the social brain—are activated.

Recent work suggests that juvenile play fighting induces the release of chemical growth factors in these areas of the brain, which may promote growth and development of these areas (Gordon, Burke, Akil, Watson, & Panksepp, 2003).

Among those areas whose growth is promoted is the orbitofrontal cortex (OFC), a brain area known to be involved in social discrimination and decision making.

Not unlike rats reared under conditions of play deprivation, rats with damage to the OFC fail to modify their behavior appropriately with different social partners, whether in playful or non-playful contexts.

That is, although rats with OFC damage can execute appropriate actions, these actions are not modified to take into account the idiosyncratic features of the partner’s social status or its movements (Pellis et al., 2006).

Findings from several laboratories indicate that the juvenile-typical pattern of play fighting produces experiences that provide feedback for some of the brain areas responsible for generating such play and so promotes development of those areas.

That such feedback may actually lead to functional enhancement in the output of these brain areas as the rats mature is suggested by deficits seen in rats with OFC damage and those with intact brains that have been deprived of play-fighting experience as juveniles.

Furthermore, these brain areas are many of the same areas that regulate social behavior and cognition in general, and so improvements derived from play fighting may improve the capacity for more subtle social interactions.

Conclusion

The broad outlines of the story for laboratory rats suggest that there is a mechanism by which experiences accrued during play fighting can improve social competence.

There is good evidence that there is continuity between human and nonhuman animals for at least some forms of play (Power, 2000), especially play fighting (Panksepp, 1998).

There seems to be a considerable similarity between the behavioral effects of play deprivation in the early development of monkeys and that described here for rats (for a review, see Pellis & Pellis, 2006).

If a similar pattern exists for rats and nonhuman primates, it is plausible that, for humans also, experience in play fighting in childhood is causally related to social competence later in life.

Thus, the correlation between experience in play fighting and social competence in humans (Pellegrini, 1995) may not be spurious. That is, it may not be the case that the more socially competent children engage in more play fighting, but rather that the play fighting may promote the development of social competency.

Given the value of the rat model for studying the role of play fighting in the development of the social brain and social competence, it can be further used to elaborate the causal mechanisms involved.

For example, researchers can characterize not only the broad areas of the brain that are altered by play experience but also the actual neural mechanisms by which the brain’s structure and function are modified by such experience.

Similarly, the facets of the play-fighting experience most important in promoting the development of the social brain can be characterized.

Finally, it has been well established for humans and nonhuman animals that play fighting is more frequent and rougher in males (Power, 2000).

The rat model can help researchers determine whether the juvenile experiences needed to develop the social brain differ between the sexes and, if so, how.

Again, rats provide a means with which to conduct the critical experiments that are either not practical or not ethical with humans. The knowledge thus gained can provide the clues to the correlated consequences of those processes that can be studied in humans.

Sources and References —

Bjorklund, D.F., & Pellegrini, A.D. (2002). The origins of human nature: Evolutionary developmental psychology. Washington, DC: Ameri-can Psychological Association.
Burghardt, G.M. (2005). The genesis of animal play. Cambridge, MA: The MIT Press.
Diamond, A. (2000). Close interrelation of motor development and cognitive development and of the cerebellum and prefrontal cor-tex. Child Development, 71, 44–56.
Einon, D.F., & Morgan, M.J. (1977). A critical period for social isolation in the rat. Developmental Psychobiology, 11, 213–225.
Gordon, N.S., Burke, S., Akil, H., Watson, S.J., & Panksepp, J. (2003). Socially-induced brain ‘‘fertilization’’: Play promotes brain derived neurotrophic factor transcription in the amygdala and dorsolateral frontal cortex in juvenile rats. Neuroscience Letters, 341, 17–20.
Panksepp, J. (1998). Affective neuroscience. New York: Oxford University Press.
Pellegrini, A.D. (1995). Boys’ rough-and-tumble play and social competence: Contemporaneous and longitudinal relations. In A.D. Pellegrini (Ed.), The future of play theory: A multidisciplinary inquiry into the contributions of Brian Sutton-Smith (pp. 107–126). Albany: State University of New York Press.
Pellis, S.M., Field, E.F., & Whishaw, I.Q. (1999). The development of a sex-differentiated defensive motor pattern in rats: A possible role for juvenile experience. Developmental Psychobiology, 35, 156–164. Pellis, S.M., Hastings, E., Shimizu, T., Kamitakahara, H., Komorowska,
J., Forgie, M.L., & Kolb, B. (2006). The effects of orbital frontal cortex damage on the modulation of defensive responses by rats in playful and nonplayful social contexts. Behavioral Neuroscience, 120, 72–84.
Pellis, S.M., & Pellis, V.C. (1987). Play-fighting differs from serious fighting in both target of attack and tactics of fighting in the lab-oratory rat Rattus norvegicus. Aggressive Behavior, 13, 227–242. Pellis, S.M., & Pellis, V.C. (1998). Play fighting in comparative perspective: A schema for neurobehavioral analysis. Neuroscience & Biobehavioral Reviews, 23, 87–101.
Pellis, S.M., & Pellis, V.C. (2006). Play and the development of social
engagement: A comparative perspective. In P.J. Marshall & N.A. Fox (Eds.), The development of social engagement: Neurobiological perspectives (pp. 247–274). Oxford, England: Oxford University Press.
Pellis, S.M., Pellis, V.C., & Foroud, A. (2005). Play fighting: Aggression, affiliation and the development of nuanced social skills. In R. Tremblay, W.W. Hartup, & J. Archer (Eds.), Developmental origins of aggression (pp. 47–62). New York: Guilford.
Power, T.G. (2000). Play and exploration in children and animals.
Mahwah, NJ: Erlbaum. Von Frijtag, J.C., Schot, M., van den Bos, R., & Spruijt, B.M. (2002).
Individual housing during the play period results in changed re-sponses to and consequences of a psychosocial stress situation in rats. Developmental Psychobiology, 41, 58–69.