The Playful Brain

Venturing to the Limits of Neuroscience

Sergio Pellis, Vivien Pellis

• Publisher: Oneworld Publications
• Year: 2013
• ISBN:
  9781780744629
• Topic: Psicología
• Subtopic: Neuropsicología

A groundbreaking study into the formative role of play in our lives Sergio and Vivien Pellis have synthesized three decades of empirical research to create a remarkable work, unequalled in its field.
A book that will not only expand our current knowledge of play behaviour, but will inspire change and progress from the laboratory to the playground.

1

THE PUZZLE OF PLAY

Mbundi runs up to Ntondo from behind. As he runs past, he grabs Ntondo by the arm. Ntondo jerks his body back, and braces against being pulled forward. This brings Mbundi to a standstill, facing Ntondo. After looking at each other for a moment, Ntondo turns his head and lunges, with his mouth wide open, and bites Mbundi’s hand, which is still holding Ntondo’s arm. As Mbundi releases his hand and withdraws it, he lunges forward, grabs Ntondo by both shoulders and bites at the side of his neck. Ntondo ducks and rolls onto his side, Mbundi follows and falls on top of Ntondo. They grapple with one another, delivering gentle bites wherever they can. Eventually, Mbundi jumps up and begins to run away, but then slows down, and, with a wide-open mouth, looks back over his shoulder. At first, Ntondo is slow to stand up, but he then jumps to his feet, and chases after Mbundi.¹

The preceding description of what many observers would call “rough-and-tumble play” or “play fighting,” in two juvenile gorillas, could fit any number of primates, or with a reduction in the role of the hands, almost any mammal. Roughhousing play such as this is familiar to most readers through their children, recollections of their own childhood in the schoolyard, pet cats and dogs that they may have reared, or from monkeys and apes seen at the zoo. But what is it that is playful about this behavior?

Play fighting is but one form of play, a behavior that can also involve objects, such as a kitten playing with a ball of wool, or one that is self-directed, such as a calf gamboling in a meadow. If we consider human children, play can also involve playing peek-a-boo or donning a superhero costume and fantasizing. Therefore, the range of behavior that can be labeled as play is quite extensive, especially when considering humans.² So what are the characteristics that define behavior as play? Historically, defining play has not been an easy task, and there is no single agreed-upon definition. Nevertheless, there are criteria that most researchers generally agree to be necessary components of a definition of play: it is an activity that is engaged in voluntarily, and it is positively reinforcing – that is, the performers find it pleasurable. Although these two criteria are true of other behaviors, such as eating and sex, another commonly incorporated criterion is that the purpose of play is not immediately utilitarian. This feature of play is often critical, since for non-human animals, play is often a simulation of a functional activity, such as fighting or predation. Thus, it is the absence of the normal consequences of these behaviors – the killing and eating of prey or the taking of food or some other resource from a social partner – that alerts the observer to the possibility that the behavior being observed is play.

There is an overabundance of definitions posited for play, with much of the confusion and argument arising from the different perspectives of various authors. For example, some authors have focused on the properties of play behavior, such as its seemingly exaggerated movements, while others have focused on the outcomes of the behavior, such as whether it simulates sex or aggression. Some definitions that emphasize a specific property of play, such as its lack of immediate function, have been the most widely adopted, but they run the risk of being so general that most behaviors that are performed by immature animals could result in being characterized as play. Therefore, in most cases, we rely on our intuition to distinguish between play and non-play.³ However, the less like humans the species being observed are, the greater the likelihood that our intuition may lead us astray.

For example, are two immature cockroaches pushing and lashing each other with their antennae, for what seems like no apparent purpose, exhibiting play? Unlike the case of two puppies play fighting, we are not privy to a body language that makes sense to us – for puppies, wagging tails, floppy ears, and a relaxed body tone are most often the clues that we use to distinguish such behavior from serious aggression. We use similar clues from body language when trying to decide whether two children are playing or fighting. When videotaped sequences of play fighting and serious fighting are shown to children and to adults, both use a variety of clues ranging from whole body movements to facial expressions in order to be able to differentiate between the two behaviors. Because there are multiple cues that can be used to distinguish between playful and serious fighting, if faces are not visible, other features of the body movements can instead be used. Obviously, the more acquainted observers are with the species in question, the more likely they are to have access to a range of criteria, whereas the more alien the species, the more limited the criteria. In addition, when studying human play, subjects that are engaging in either playful or serious fighting can, of course, be asked as to whether their behavior was playful or serious, so as to verify the judgments of the observers that are based on the behavioral cues alone.⁴ However, even this last item is not foolproof, as humans are notorious for telling untruths: after all, how often do we smile when we are really not happy? Nonetheless, when trying to decide whether the behavior of species other than human should be labeled as play, no such additional information, however suspect, is available. Yet, in order to comprehend the problem of play fully, we need to know which borderline cases in the animal kingdom belong to the play category and which do not.

Developing a more exhaustive range of criteria that can readily distinguish between the playful and non-playful behavior of all animals, be they immature or adult, has two advantages: it brings the non-human literature into closer correspondence with the human literature, and it enables us to compare a diverse range of animals. For example, Gordon Burghardt has developed a set of criteria that must be met for an instance of behavior to qualify as play: (1) that the behavior is incompletely functional in the context expressed; (2) that it is voluntary; (3) that it is, in some ways, structurally modified or temporally shifted as compared to when it is used in its normal, functional context; (4) that it is performed repeatedly, but not necessarily in an invariant form; and (5) that it is present in healthy, unstressed animals. In using these five criteria, researchers have shown that animals as diverse as turtles, wasps, and octopuses engage in behavioral sequences that are comparable to those performed by mammals such as dogs and monkeys – ones to which most observers would happily apply the label of play.⁵ Unfortunately, in most cases, the lack of detailed data means that comprehensive comparisons across the entire animal kingdom so as to determine the presence of play limit our attempts to plausible best guesses.

However, if we just focus on the cases where most observers would agree that what they are seeing is play, we are still left with an interesting phenomenon – that the majority of mammals and many birds spend some of their time in a seemingly pointless behavior. Based on studies of both free-living and captive animals, play occupies up to 20% of an animal’s daily time budget and up to 10% of their daily energy budget. Given that these figures are for animals in their juvenile period, this implies that these individuals are sacrificing resources that could be channeled into growth. Furthermore, when playing, animals risk making themselves conspicuous to predators and chance injury. Although there is debate about how significant a burden these costs may actually be, there is little doubt that play involves some cost, such as spending less time feeding, and so must also have some compensating benefits – even if these benefits are modest in magnitude.⁶

Commensurate with the breadth of human imagination, there is a long list of proposed benefits of play. Most are predicated on the view that, because play has no immediate purpose, the benefits are delayed. That is, juveniles play so as to become better adults. Occasionally, scholars have been drawn to the possibility that play may serve to build a better juvenile⁷ – but this would then imply an immediate function, which creates more problems for the definition of play. To make matters worse, some have posited that in most cases, what is labeled play serves no function whatsoever, be it delayed or immediate. If play is a property of immaturity, then how immature organisms attempt to perform actions may, from an adult observer’s point of view, appear playful. In this scenario, play is an epiphenomenon of processes enacted in the immature stages of development, and it is these processes that need explanation, not the incidental by-products of such processes.⁸ There is good reason why these views sound confusing and even contradictory to us. Like all biological traits, play has evolved, and evolution is a messy process. The origin of traits need not reflect their current functions, and traits used for one function at a particular time may be co-opted for another function at another time. For example, two adaptations associated with modern birds are long, hollow bones and wings that use feathers as an aerofoil. Yet the origins of feathers pre-date birds – dinosaur ancestors likely used feathers for insulation, not flight, and hollow limb bones seem to have pre-dated even dinosaurs with feathers.⁹ This is also likely to be true for play.

There is no doubt that many properties of animals (such as being “hot-blooded” or “cold-blooded”), and developmental processes (such as the piecemeal maturation of sensory and motor capacities), are, when brought together in a particular combination, likely to generate play-like behavior. Such play-like behavior may be functionless, but once present, it could then be co-opted for some useful function, with those features that are the most important to that function being honed to serve that function better. At some future point, that modified play behavior may again be co-opted for another function and so undergo more changes appropriate for the new function. Some lineages of currently playful organisms may reflect any or all of these levels of transformation.¹⁰ It is this complex tapestry created by millions of animals evolving over vast periods of time that causes us to stumble when we try to encapsulate these diverse patterns and processes into a single definition or explanatory theory of play. But this very richness in variation is also an advantage. Nature has provided us with a vast array of natural experiments, with different lineages of organisms having changed play in this way or that, which allow us to exploit this variability as a useful tool for research.

However, the downside of using natural diversity is in making sure that what is being compared is indeed comparable. For example, if species A plays in a complex manner with sticks or other inanimate objects, and species B does so with other members of its species, is the play comparable? Even if we only compare play that occurs between members of the same species, can we be sure that the play-like fighting in cockroaches bears any relation to that of gorillas? Our solution to this problem is to focus attention on just one form of play, and to do so by examining how it varies in just one lineage of related animals. In the comparative literature, play fighting, or rough-and-tumble play, is the most commonly reported form of play. And, within that literature, the most detailed and extensive experimental research has focused on laboratory rodents, with the rat being especially prominent.¹¹ Furthermore, there is sufficient detail available on a dozen or so rodents for us to determine what features of play fighting are unique to rats and what features of play fighting are shared across several species of rodents. A comparative analysis allows us to identify those features of play fighting that may be generalized to all species that engage in play fighting. What we learn from rats can then be applied to species closer to our hearts and minds, such as ourselves. In addition, the approach advocated here is informative in another way.

Comparisons among closely related species can provide clues as to what features can be changed independently of one another and how those changes may be related to the novel functions that play may have for that species. Also, the identification of those changes can lead to useful hypotheses about the accompanying brain changes needed to enact such a behavioral change. So, the first task of the comparative analysis that we use here is to chart the pathway by which a particular species has come to acquire its unique characteristics of play fighting.¹²

There is also another benefit in using the comparative approach. Once the unique features of a trait are identified in some species in one lineage of related species, the net can be cast more widely to see if other lineages have sprouted species with similar characteristics. Of all of the rodent species that have been studied, rats have evolved the most complex pattern of play fighting, with control mechanisms over play that resemble those seen in other lineages, such as primates. In some features, the play fighting of rats closely resembles that which is present in humans and in related non-human primates.¹³ When traits in species from two different lineages converge in such a manner, it is likely that those features have evolved in both of them to solve similar problems. This convergence offers two advantages to the researcher. First, we can use the comparison to help identify what the common social or environmental problems may be that facilitate the evolution of such traits. Second, we can identify species that may be good models for the experimental analysis of that trait. As we shall see, because the play fighting of rats shares at least some features in common with the play fighting of humans, we have an avenue available to study those traits in a way that cannot be done with human subjects.

Our laboratory has made two primary contributions to this endeavor. First, we examined, in detail, the play fighting in rats and many other rodents and characterized the key components of this behavior (see above). Second, in a series of experiments, we showed that the cortex, the most evolutionarily advanced part of the mammalian brain, is not necessary for rats to engage in play fighting. That is, rats without a cortex (decorticate) are still able to use all the behavior patterns typical of play fighting and to engage in such play just as frequently as rats with intact brains. Consequently, decorticate rats not only want to play, but also know how to play. However, when they play, their behavior is not without abnormalities. These rats fail to modify how they play at different ages; rather, at all ages, they play in the same manner. Nor do they modify their play when interacting with different partners – they play in the same manner whether their partner is a dominant male, a subordinate male, or a female. Furthermore, these age-related and partner-related modifications in play fighting involve different neural circuits in the cortex, as we will explain in greater detail in a later chapter. Thus, there are distinct cortical and subcortical controls over play fighting in rodents, with some species having all the control mechanisms and others having few or even none. Based on this framework, we can use the comparative data set to ask the question: “How can a brain, capable of producing play fighting, be constructed from one that cannot?”

A Cause for Rejoicing and A Cause for Caution

The rat thus provides a tool by which to chart the evolution of play fighting. As there is more known about the brain and be...