How Play Makes for a

More Adaptable Brain

!#OMPARATIVEAND.EURAL0ERSPECTIVE
s
Sergio M. Pellis
Vivien C. Pellis
Brett T. Himmler
Studies of rats and some primates show that rough-and-tumble play among juve-
niles improves social competence, cognition, and emotional regulation later in
life. Most critically, such play makes animals better able to respond to unexpected
situations. But not all animals engage in play, and not all animals that play appear
to gain these benefits. Using a model developed by Burghardt (2005), the authors
argue that there are enabling conditions—such as how behavior systems develop
and the presence of surplus resources—that make play-like behavior possible.
Once such behavior emerges, other enabling conditions help transform it into
more exaggerated patterns of play that can be co-opted for various functions.
For species living in complex social systems with an extended juvenility, play has
become a tool to refine the control that the prefrontal cortex has over other neural
circuits. Such control permits these animals to have more nuanced responses to a
variety of situations. In short, the juvenile experience of play refines the brain to
be more adaptable later in life. Key words: comparative studies; developmental
benefits of play; play and adaptability; play in the animal kingdom

Introduction

There is growing experimental evidence that play in rats, especially social

play, serves an important developmental role. It helps refine social skills (Byrd
and Briner 1999; van den Berg et al. 1999), improve the regulation of emotions
(da Silva et al. 1996; von Frijtag et al. 2002), and enhance executive functions
(Baarendse et al. 2013) by modifying the neural mechanisms that underlie them
(Bell, Pellis, and Kolb 2010; Himmler, Pellis, and Kolb 2013). Data on several
primate species (e.g., Kalcher-Sommersguter et al. 2011; Kempes et al. 2008),
including humans (Lindsey and Colwell 2013; Pellegrini 1995), are consistent
with these findings. In essence, the experience of play in the juvenile period pro-

73

American Journal of Play, volume 7, number 1 © The Strong

Contact Sergio M. Pellis at pellis@uleth.ca
74 AMERICAN JOURNAL OF P L AY sFALL 2014

vides a context within which young animals can experience loss of control and
deal with unpredictable events (Pellis, Pellis, and Foroud 2005), but do so in a
rewarding setting (Panksepp 1998; Vanderschuren 2010). This appears to enable
animals to train to deal with the unexpected vicissitudes of life (Pellis, Pellis,
and Reinhart 2010; Špinka, Newberry, and Bekoff 2001). But before we explore
how such play-induced brain changes can help make animals better at dealing
with the life’s uncertainties, we need to answer a more fundamental question.
We should be bear in mind that the animal kingdom consists of about
thirty phyla that represent major groupings based on the unique features of
each phylum’s body plan. Consider the difference in body organization between
an insect like an ant and a vertebrate like a dog. The division of body parts, the
number and placement of the legs, the location and organization of the ner-
vous and circulatory systems all differ in fundamental ways (Tudge 2002). An
exhaustive review of the literature has shown that play occurs in only five of the
thirty phyla (Burghardt 2005). For example, play appears in many species in the
phylum Chordata, which includes people, dogs, and ravens and some species
of the phylum Arthropoda, which contains insects (like ants), crustaceans (like
shrimp), and arachnids (like spiders). We dot not find play, however, in the
phylum Echinodermata, which contains starfish and sea urchins, or the phylum
Annelida, which includes earthworms and leeches. Indeed, even in the phyla
containing species that play, not all the species in those phyla play. For instance,
researchers report that in Chordata only some in the subphylum Vertebrata
(those creatures with a vertebral column like humans and fish) play, and among
these vertebrates, play seems fairly common in many lineages of mammals, less
common but present in some lineages of birds, but rare among other groups
like amphibians, reptiles, or fish. In this context, we are left to wonder why play,
which seems important to training some animals to be more adaptable and
resilient, is so rare in the animal kingdom?
This rarity, rather than impeding our understanding of the origins and
functions of play, may actually prove useful to it. Consider rough-and-tumble
play (or play fighting) alone. When we examine it within a particular group
of animals, such as the rodents, we find it absent in some species and present
in others, and where present, it can range from simple to complex (Pellis and
Iwaniuk 2004). In play’s simplest form, one animal attacks another, who does
not respond (Wilson 1973). Added complexity arises when the defender flees
from the attacking partner (Pellis and Pasztor 1999). Still greater complexity
comes with the defender holding its ground as it wards off the attack, but this
 How Play Makes for a More Adaptable Brain 75

too can vary in complexity, as some species are more likely to adopt defensive
actions that promote close-quarter wrestling (Pellis, Pellis, and Dewsbury1989).
On top of these gradations in complexity, there are also differences in frequency
across species: even those having the most complex patterns do not necessarily
use them with the same frequency (Pellis and Pellis 1998a). How does all this
diversity map onto the functions of play?
As a useful organizing principle, we recognize that not everything we call
play has a function and that even those forms of play that are functional have
many different functions. Before delving much further into this issue, we should
make clear what we mean by function in a biological sense. When we consider a
trait—whether a behavioral trait like play or an anatomical trait like the horns
of a goat—in terms of the functions it serves, we look primarily at how the trait
contributes to an animal’s survival and reproduction. In an evolutionary sense, we
call traits functional if they increase the “fitness” of the possessor, such as giving the
animal a reproductive advantage over its competitors. That trait may do so indi-
rectly, by enabling the possessor to survive longer and thus enjoy more opportuni-
ties to breed, or it may do so directly, by making the possessor, for example, better
at winning mates or rearing young. However, when we use the word “function”
in more colloquial parlance, we tend to mean something different. For example,
when we eat that extra slice of Thanksgiving pumpkin pie, we do so because it is
delicious, not because we are hungry. So eating functions to increase our pleasure.
In the context of play, we may say animal A performs X during play because the
animal finds it pleasurable to do so, meaning that the function of the behavior is
to induce pleasure. We resolve these divergent usages of the term “function” by
recognizing that we do pleasurable things because for our ancestors pleasurable
activities generally increased their fitness (eating and having sex come to mind).
Pleasure seems to induce us to do things, like play that increase our fitness.
While most functional accounts of play focus on the way play in juveniles
produces better functioning adults (Baldwin 1986; Fagen 1981), this emphasis on
the young neglects the considerable play in which adults engage (Cohen 2006).
Yet in some lineages of animals that play, such as the order of primates (to which
we, chimpanzees, and rhesus monkeys belong), adults continue to play in 50
percent or more of species (Pellis and Iwaniuk 1999, 2000a). Some comparative
evidence shows that when adults play, the play can have several immediate func-
tions, such as regulating intragroup and intergroup tensions (Palagi 2011) and
enabling them to navigate dominance relationships (Pellis 2002). Thus, some
functions of play offer immediate, rather than delayed, benefits.
76 AMERICAN JOURNAL OF P L AY sFALL 2014

When researchers focus on delayed functions, the difficulties increase, as

it becomes more problematic to decide which adult skills to compare with the
purported gains made from juvenile play. Indeed, associations that seem prom-
ising in one species evaporate when researchers study another species, leading
some to a dismal view of play as having minimal or modest benefits at best
(Martin and Caro 1985). For example, a recent paper on play and development
in free-living marmots has shown a convincing correlation between juvenile
play and a later capacity to gain dominance (Blumstein et al. 2013), and work
on free-living bears has found that cubs that play more are also more likely to
survive to weaning (Fagen and Fagen 2004). But detailed studies of free-living
meerkats (an African species of social mongoose) that specifically tested these
functions, among others, found no support for them (Sharpe 2005a, b, c; Sharpe
and Cherry 2003). The paucity of evidence and the conflicting support provided
for the different functions of play add to the problems raised by the absence of
play in much of the animal kingdom and to the variation in the complexity of
play seen in the species that engage in it (Burghardt 2005; Pellis and Pellis 2009).
The comparative evidence clearly shows that play is not a unitary trait,
neither does it have a clear and singular function. Talking about play in this
way seems to lead to pointless arguments about the supposed benefits of play
(Fagen 1981; Martin and Caro 1985). In our view, the best way to address the
conceptual and empirical difficulties created by the absence of play in so many
branches of the animal kingdom (and by the diversity in the patterns of play
among those species that do play) and to pinpoint the illusive functions of play
is to examine the variability in the structure and function of play in a historical
context. This perspective recognizes that, within lineages, patterns considered
as play may have undergone unique transformations, with different functions
becoming possible with different kinds of transformations (Burghardt 2005;
Pellis and Pellis 2009). For example, the play of cats has a stronger link to the
underlying motivations associated with predation (Hall 1998) than does the play
of dogs, in which stronger social influences pervade (Biben 1982).

The Origins and Multiple Transformations of Play

Compare two juvenile chimpanzees engaged in play fighting and two immature
cockroaches tussling for no apparent reason. Most readers would have little dif-
ficulty labeling the behavior of the chimpanzees as play, but they would most
 How Play Makes for a More Adaptable Brain 77

likely label that of the cockroaches as some form of immature aggression (Fagen
1981). With examples like these in mind, Burghardt (1984, 1988) has deliberately
focused on the borderlines of play, those cases with elements of behavior that,
observed in a mammal, would be called play, but observed in non-mammals,
would probably not be called that. This focus on borderline cases led to two
major breakthroughs (Burghardt 2005). First, Burghardt developed a compre-
hensive definition of play as behavior that meets five criteria. These are: (1) the
behavior should not be completely functional in the context in which it occurs,
(2) it should be voluntary, (3) it should be modified in some way compared
to its normal occurrence in a functional context, (4) it should be performed
repeatedly but not necessarily invariantly, and (5) it should appear in healthy,
unstressed animals. In applying these criteria, researchers have shown that not
only does some behavior in mammals—such as dogs and monkeys—qualify as
play, but that some behavior in animals as diverse as turtles, wasps, and octopus
also does so (e.g., Dapporto, Turillazzi, and Palagi 2006; Kramer and Burghardt
1998; Kuba et al. 2006). Indeed, as we already noted, the rigorous application of
these criteria has led to identifying play in a wide range of animals from several
phyla. However, this still leaves play unidentified in most phyla and, again, as
we noted, not all lineages of species within phyla in which play occurs exhibit
behavior that can be considered play.
Clearly, play seems relatively rare in the animal kingdom, and the fact that
it appears among distantly related phyla implies that play must have arisen
independently many times (Burghardt 2005). These comparative data confirmed
a hypothesis that the conditions enabling play to arise are multiple and likely
occur only in peculiar circumstances (Burghardt 1984, 1988). Moreover, in
many cases, these enabling conditions create play that is barely recognizable as
play; yet, in some lineages, the play is so spectacular and exaggerated that few
observers, if any, would refuse to call it play. Indeed, to recognize the play of
some turtles as being play, Burghardt had to speed up the film he watched. No
such speeding up of the film is necessary to recognize the play of otters. Thus,
first, we have to overcome our own prejudices and limitations as observers, but
when we do we need, second, to recognize that not all the play we observe is the
same. In short, some cases that fit Burghardt’s criteria, just barely do so, whereas
others do so completely.
These considerations led to Burghardt’s second major insight. Play arises as
a byproduct of enabling conditions, producing an incipient or play-like form of
behavior that may be borderline in qualifying as play (primary-process play). But
78 AMERICAN JOURNAL OF P L AY sFALL 2014

once such play is present, further conditions may exaggerate its frequency or its
content making it more recognizably play (secondary-process play). Additional
enabling factors may lead to even more exaggerated behavior unquestionably
related to the play category (tertiary-process play). That is, in this historical
perspective, the conditions for the origins of play can be characterized and dis-
tinguished from the conditions that may act to transform play further (figure
1). Moreover, even though in its origins, play may have arisen as a byproduct
of propitious circumstances and so without any functional benefits, once such
behavior existed, the various transformations that then accrued could have cre-
ated the conditions for novel functions to arise (Burghardt 2005).
The broad comparative view of play, then, reveals a diverse range of phe-
nomena encompassed within the label of play. Different lineages have evolved
play-like behavior, and then some of those lineages have further transformed
that behavior into patterns of play that serve particular functions. Importantly,
this framework allows for those functions to be multiple and disparate, with
some overlapping due to convergence and some differing due to divergence.
Certainly, this framework can account for both the presence and absence of play
in the animal kingdom and for the complex array of functions that it can sup-
port. Comparative research on variations in the social play of rodents provides
examples of each of these kinds of transformations as envisioned by Burghardt’s
theoretical schema.

The View from Rodents and Their Play Fighting

Rodentia is the largest order of the class Mammalia, consisting of about 40 per-
cent of all mammal species. For example, there are about two thousand species
of rodents, but less than three hundred species of primates. The rodents are
divided into three major subgroups; the rat-like or mouse-like rodents (murid
rodents) are the most abundant, comprising about 50 percent of all rodent spe-
cies (e.g., rats, mice, gerbils, and hamsters). The other two groups consist of the
squirrel-like and the guinea pig-like rodents (Nowak 1999). Detailed analysis of
play fighting in murid rodents shows that play is not distributed in a uniform
manner (Pellis and Pellis 1998a). In this group, such play can be absent, and, if
present, can be simple, complex, or something in between. Given their differ-
ing patterns of relatedness to one another, the possible transformations in the
content of play can be traced. To do so, we need a specialized approach from
 How Play Makes for a More Adaptable Brain 79

Figure 1. Sequential transformations of play over evolutionary time and

their enabling factors (Burghardt 2005, reprinted with permission)

comparative biology, and this needs some explanation.

Species can be placed on a tree diagram (i.e., a cladogram) that shows the
pattern of relatedness among the set of species. Importantly, cladograms do
not claim ancestor-descendent relationships among the species, rather, all the
80 AMERICAN JOURNAL OF P L AY sFALL 2014

species appear on the terminal branches with species linked to one another at
nodes, which represent bifurcation points at which presumed ancestors have
diverged into the daughter species (Hennig 1966). Placing the murid species
on a cladogram, the degree of complexity of the play fighting performed can be
mapped. In doing so, using the assumption of parsimony so that the tree shows
the fewest transitions possible, the pattern of transformation in the lineage and
branches of the lineage can be determined (figure 2).
The cladogram shows two important patterns. First, the most likely ances-
tral state suggests the animals have moderate levels of complexity in their play
(dark stippling). Second, the terminal branches show that extant species have
either exaggerated that complexity (black for most complex, grey for next most
complex) or reduced it (light stippling for simplified play, white for play being
absent or near absent). Consistent with Burghardt’s framework, the cladogram
of the rodents shows that play changes in form over evolutionary time with
different lineages transforming play in different ways. The elimination of play
shown in some lineages also proves telling. While the costs—small, moderate,
or large—of playing have been debated (Martin and Caro 1985), specific cases
have emerged that suggest play can be costly, indeed. For example, in free-living
chimpanzees in West Africa, play fighting appears as a means of transmitting
lethal infectious diseases, which, in some years, may lead to a major culling of
juveniles (Kuehl et al. 2008). Again, whether the costs sustained are small or
large may depend on whether a particular lineage has co-opted play for some
critical fitness-enhancing function. Sustaining larger costs suggests larger coun-
terbalancing benefits for play to be maintained in the population. The rodent
cladogram indicates that if the benefits are insufficient, play will be eliminated.
Broadening the comparative framework to include the other major subdi-
visions of rodents (Pellis and Iwaniuk 2004) and embedding rodents with the
other orders of mammals (Burghardt 2005) suggests that the ancestral group
giving rise to the rodents either did not play or had a very rudimentary pattern
of play. Using this pattern as a starting point to consider the variation across
extant species of rodents, a rough framework can be developed for the kinds of
play envisaged in Burghardt’s primary, secondary, and tertiary processes. How-
ever, we must keep a caveat in mind: such a framing of extant species does not
represent the true pattern of evolutionary change, since, as shown in figure 2,
there have been losses as well as gains. Nonetheless, the play in the extant spe-
cies can be ordered in a manner that conceptually illustrates the kind of grades
of organization and transformation envisaged by Burghardt’s model (figure 1).
 How Play Makes for a More Adaptable Brain 81

Figure 2. Complexity of play fighting and its evolution for murid rodents
(Whishaw et al. 2001, reprinted with permission)

Among murid rodents, play fighting primarily involves the simulation of

precopulatory behavior, in which partners compete for access to the body targets
that are contacted during adult sexual encounters. For example, rats compete to
82 AMERICAN JOURNAL OF P L AY sFALL 2014

contact and nuzzle the nape of the neck, and Djungarian hamsters compete to
lick and nuzzle the partner’s mouth, whereas during serious aggression, these
species attempt to bite each other on the rump and lower flanks (Pellis 1993).
Despite these similarities, there are species differences in the degree of similar-
ity of the playful version of this behavior to the adult, functional version (Pellis
and Pellis 1998a). Importantly for the evolution of play, the developing behav-
ioral system changes in a piecemeal manner, which, without regulatory control,
can be expressed precociously. Add to this an environment offering protection
against predators and abundant resources provided by parents, and the likeli-
hood of precociously performed behavior increases—and may do so to the level
in which it begins to meet the criteria for it to be labeled as play (Burghardt
2005). Therefore, for some rodents, when the behavior closely resembles the
expression of precocial sexual behavior, we may think of it as play-like behavior,
or incipient play (figure 3). Such an origin would be consistent with Burghardt’s
primary process play. Once the presence of this fragmented, immature behavior
becomes a reliable part of the experiential world in which the animal develops,
it can substitute for maturational processes that are otherwise insensitive to
experience. This second stage may not involve any modifications to the content
of the immature behavior expressed, but simply by its increased frequency of
performance, such behavior in the juvenile stage could nonetheless provide
essential, experiential feedback for wiring the brain, and so, at least functionally,
may be thought of as rudimentary play fighting rather than simply as immature
behavior (figure 3). This, then, reflects a transformation that would make the
play more like Burghardt’s secondary-process play.
A further transformation can arise by modifying the content of the juvenile
version of adult sexual encounters. For example, if the majority of the beneficial
experiences derived from play fighting occurs when the animals are wrestling one
another, then increasing the frequency of the tactics of attack and defense that
increase the frequency of wrestling would be advantageous, and, in the absence
of countervailing costs, would be selected for, and the organization of the play
would, over generations, change to that we see in the adult sexual encounters.
Once modifications have been made to the organization of play fighting itself,
not only would this behavior facilitate the development of sex, but it also would
become an essential component of the normal developmental experience. Thus,
with this third step, the playful interactions become both quantitatively and
qualitatively different from sexual interactions and the label of rudimentary
play seems insufficient and would be better labeled true play fighting (figure 3).
 How Play Makes for a More Adaptable Brain 83

Behavior and context Consequences and functions Classification

Components of sexual None Incipient play

behavior, especially (i.e., play-like behavior)
precopulatory elements.
These are expressed in a
precocious manner during
the juvenile period.

Under appropriate Precopulatory behavior Rudimentary play fighting

conditions, precocious becomes necessary for
sexual behavior becomes the maturation of normal,
a frequent and expected adult sexual performance.
component of the juvenile
period. However, at
this stage, the juvenile
interactions differ
little from adult sexual
interactions.

Some components of These elaborations ensure True play fighting

precopulatory sexual that the necessary sexual
behavior are elaborated skills are acquired during
during the juvenile period, the juvenile period.
making the interactions
more clearly different from
adult sexual behavior

Under some conditions, These patterns of Emancipated play fighting

this sexually derived interactions now serve
pattern of play fighting nonsexual as well as sexual
is modified to a more functions.
exaggerated degree and
co-opted into use in novel
domains of juvenile and
adult life

Figure 3. Hypothetical stages in the transformation of immature sexual

behavior into play fighting in murid rodents (adapted from Pellis 1993,
reprinted with permission)
r murid rodents

This transformation is more consistent with Burghardt’s tertiary-process play.

Note that in the model, what has transpired is that, through successive
changes, precocial sexual behavior has been transformed into playful behavior,
functioning to promote the development of sexual skills. In rats, the organiza-
84 AMERICAN JOURNAL OF P L AY sFALL 2014

tion of play fighting is more greatly modified than in any other murid rodents
so far studied (Pellis and Pellis 1998a), which suggests another layer of trans-
formation. Juvenile play in rats has been further modified, so that it not only
facilitates the development of sexual behavior but also the promotion of social
competence beyond the sexual domain. Even more strikingly, play fighting itself
is retained into adulthood as a tool for social assessment and manipulation (Pel-
lis and Pellis 2011). Because of the novel organizational changes as well as its
expansion beyond its original function in sexual development, this form of play
fighting requires a different label, emancipated play fighting (figure 3). It may
be merely semantic whether such a transformation corresponds to an advanced
tertiary-process play or represents an addition to Burghardt’s original formula-
tion, quaternary-process play. What is important is that new transformations
are laid over past transformations with new functional opportunities emerging
as further transformations are made.
The evidence supporting these various transformations in the play of
rodents have been detailed elsewhere (Pellis and Pellis 2009); the key message to
take from this brief review is that, when viewed comparatively, play has multiple
levels of organization and potential functional uses. Thus, it is naïve to expect
that all animals that play will play similarly or gain the same benefits. That being
the case, we can go back to, and modify, our opening question: why is it that all
animals do not play to accrue the kinds of benefits shown for rats?
To understand some of these transformations, it is first necessary to have an
idea of how the vertebrate brain is organized. The brain divides into two major
components: the cerebral cortices and the remainder (Kolb and Whishaw 2009).
When we open the skull of a mammal, the largest and most obvious structure
we see is the cortex, composed of two hemispheres that cover most of the rest
of the brain. The subcortical structures lie beneath the cortical hemispheres.
These different layers have complex patterns of interconnection with the dif-
ferent networks that modify each other’s function.
To explain why rats gain so much from playing as juveniles and other
rodents do not, we need to keep several points in mind. First, the comparative
evidence clearly shows that not all rodents play in a manner comparable to rats
(Pellis and Pellis 1998a). Second, the organizational transformations present
in rats that are not shared with other rodents involve novel regulatory controls
originating in the cortex (Kamitakahara et al. 2007). Third, the higher-level cog-
nitive benefits that accrue from playing in rats are not present in other rodents
that play (Einon et al. 1981), and at least some of these cognitive benefits have
 How Play Makes for a More Adaptable Brain 85

been shown to involve changes in cortical function (Baarendse et al. 2013). That
is, in rats play has been modified to provide a novel function—that of enhanc-
ing cortical regulation of emotional and cognitive processes—especially as they
pertain to social behavior, and this has had the effect of modifying the cortical
neural circuits important to such regulation (Bell et al. 2010; Himmler, Pellis,
and Kolb 2013).
As we can see, the transformative approach to comparing play across spe-
cies yields novel insights into play because it shows that not all species that play
gain the same benefits from doing so. Moreover, the evolution of novel benefits
require changing both how the play is organized to yield experiences that are
important for shaping the development of the relevant brain mechanisms and
the capacity of those brain mechanisms to be influenced by such experiences.
Among close relatives of rats, play has been transformed in a way that has led
to divergence in the form and function of play (see figure 2). However, we have
already touched on the possibility that the higher-level transformations of play
in rats have converged with organizational and functional properties similar to
those we see in some primates. For example, the quaternary changes in the play
of rats that influence the development of executive function are similar to those
we see in humans and some other primates. Understanding that convergence
can help frame the question about how the play-induced brain changes we see
in any of these species may lead to improved adult social competency.

Convergence in Play Fighting

Most of what we know about the impact of play fighting in primates on later
social, emotional, and cognitive function comes from studies of Old World
monkeys (Kempes et al. 2008) and apes (Kalcher-Sommersguter et al. 2011).
In these groups of primates, play fighting appears primarily as a simulation of
conspecific fighting—the same body targets are bitten and the same combat
tactics are used (Aldis 1975; Owens 1975; Pellis and Pellis 1997; Reinhart et al.
2010; Symons 1978). For example, gorillas wrestle one another during both play
fighting and serious fighting to gain access to the lateral edge of the shoulder,
which is bitten if contacted (Schaller 1963). Even though the same target and
tactics are used during both play fighting and serious fighting, applying the
criteria for play established by Burghardt shows that play is not just an imma-
ture version of serious fighting. Thus, while the play fighting of rats has evolved
86 AMERICAN JOURNAL OF P L AY sFALL 2014

from precocial sexual behavior and that of the rhesus monkey and gorillas from
precocial agonistic behavior, depriving juvenile play experience in these species
not only affects the development of their sexual and aggressive behaviors, but
also has more wide-ranging effects on the development of social competency,
emotional regulation, and cognitive performance (Pellis and Pellis 2009). Both
rats and monkeys have modified their play fighting to exaggerate the experience
of loss of control and unpredictability (Pellis, Pellis, and Foroud 2005; Petrù et
al. 2008), and, indeed, it is unpredictability that provides the key experience.
In monkeys and apes, maternal interactions are critical to prepare the
young animal for engaging in, and benefitting from, play with peers at a later
age (Blum 2002; van Leeuwen, Mulenga, and Chidester 2014). These monkey
studies show that even an inanimate surrogate mother is better than no mother
at all, and, in this context, they found that a mobile, inanimate mother was
better than a stationary one. The mobile mother moved up, down, and around
the cage on an irregular schedule throughout the day. As crucially, the studies
observed that the infants initiated more play with the mobile surrogate than with
the stationary one and that they reacted to unexpected retreats and hits from
the mobile surrogate. When these monkeys were weaned and introduced into
peer groups, the monkeys that had been reared by mobile, surrogate mothers
were more outgoing and more likely to approach other animals. They made
fewer threats when they did so and paid more attention to novel social stimuli.
Moreover, when they were young adults, they were also more likely to engage in
successful copulations. Unlike those infants reared by the stationary surrogate
mothers, those reared by the mobile surrogate mothers behaved more like the
monkeys that had been reared by their natural mothers (Mason 1978).
Play fighting in rats and monkeys provides a context for experiencing the
unexpected—all the more so, since for play fighting to remain playful it has
to follow a certain rule structure. Unlike in serious fighting, where winning is
the sole object, in play fighting, the winning has to be attenuated so that some
degree of reciprocity is possible (Pellis, Pellis, and Reinhart 2010). On the rare
occasions that play fighting escalates to serious fighting in rats, one rat has used
excessive force to restrain its partner (Pellis and Pellis 1998b). However, in the
exuberance of play fighting, hits and bites may be delivered too firmly, and the
partner may resist following the rules. The problem for the animal is to assess the
situation and determine whether the excessive force was accidental or part of a
concerted pattern and so decide how to react to the infraction. At the same time,
as the animal loses control—often because of its own injection of reciprocity
 How Play Makes for a More Adaptable Brain 87

promoting movements that it performed (Pellis, Pellis, and Foroud 2005)—it

has to recoup from the mishap but to do so without using excessive force. Not
surprisingly, species such as rats and monkeys—species in which the organiza-
tion of the play has been modified to exaggerate these experiences—develop in
the absence of such play a compromised impulse control, emotional regulation,
cognitive performance, and social competency.

Play Fighting and the Development

of Executive Function

Play fighting can be cognitively and emotionally challenging because it exag-

gerates the experience of loss of control, especially given the unpredictability
that arises from having to use an implicit rule-structure (one that promotes
reciprocity) to recover from instability in rapid sequences of behavior that may
last only a few seconds. Yet these are precisely the experiences found frequently
in the play fighting of many species. Moreover, growing evidence suggests that
such experiences affect the development of the prefrontal cortex (at the anterior
end of the cortex, abutting the front of the skull), the area of the cortex known
for its role in executive function.
The term executive function here describes a collection of control processes
necessary for the organization of complex—and often goal-oriented—sequences
of movements in humans, monkeys, and rats. These include, but are not limited
to, monitoring behavior, attention, resistance to interference, behavioral inhibi-
tion, planning, decision making, and task switching (see Dalley, Cardinal, and
Robbins 2004 for a review) as well as impulse control (Baarendse et al. 2013).
Rats that have been reared in social isolation show many deficits linked
to executive function. For example, they react with heightened anxiety to fear-
ful situations (da Silva et al. 1996) and have an exaggerated stress response to
such situations (von Frijtag et al. 2002); they overreact to benign social contact
(Einon and Potegal 1991); they fail to behave submissively when confronted
by a dominant rat, impulsively moving about and leaving a safe place (van den
Berg et al., 1999); they have difficulty coordinating movements with a partner
in both sexual and nonsexual contexts (Moore 1985; Pellis, Field, and Whishaw
1999); and they are less competent in solving cognitive tasks (Einon et al. 1981).
However, before the link between play experience and executive function can
be fully developed, we must consider an important caveat.
88 AMERICAN JOURNAL OF P L AY sFALL 2014

When we rear a young rat in social isolation, we deprive it of more than

just the experience of playing with peers. The reasons to believe that a major
contributor to the isolation-induced effects on such rats arise from the absence
of play experience have been reviewed in detail elsewhere (Pellis and Pellis 2006).
So here, we present only some of the key evidence. In the juvenile period (span-
ning from weaning at around twenty-three days after birth to when they sexually
mature at around sixty days of age), rats devote about one hour of every twenty-
four–hour cycle to play. Giving an isolated rat the opportunity to interact with
a peer for one hour per day over the juvenile period proves sufficient to offset
the many negative effects of isolation on behavior and cognition. However, giv-
ing the isolated juvenile an hour per day exposure to an adult does not (Einon
and Morgan 1977; Einon, Morgan, and Kibbler 1978). Whether paired with a
juvenile peer or an adult, the juvenile rat will socialize by sniffing, grooming,
huddling, and, generally, coordinating its movements with its partner, but if
paired with a peer, the socializing also includes playing together. Thus, at least
to some extent, socializing that includes play appears to be important in rela-
tion to the deficits that arise from being reared in isolation during the juvenile
period (e.g., Arakawa 2007a, 2007b).
Using the paradigm of housing juveniles either with adults or with other
juveniles to avoid the rats being reared in complete isolation, researchers found
that the opportunity to engage in social play with one other peer is sufficient
to modify the rats’ dendritic arbor (think of branches of a tree) of the neurons
of the medial prefrontal cortex (mPFC) and that being reared with multiple
social partners, whether or not they provide play experiences, is sufficient to
modify the dendritic arbor of the neurons of the orbital frontal cortex (OFC)
(Bell, Pellis, and Kolb 2010). Moreover, such studies show that for the mPFC,
the play-induced neuronal changes result in increased dendritic plasticity when
exposed to other experiences later in life (Himmler, Pellis, and Kolb 2013). Selec-
tive lesions of the mPFC and the OFC in rats that have been reared socially as
juveniles reveal somewhat different roles for these circuits. With damage to the
OFC, rats fail to modulate their social interactions with different partners—that
is, they interact similarly with dominant and subordinate partners (Pellis et al.
2006). With damage to the mPFC, rats can modulate their play with partner
identity, but appear to have difficulty in coordinating complex movements with
their partners (Bell et al. 2009; Himmler et al., 2014). Therefore, prefrontal dam-
age mimics some of the typical social deficits from being reared in isolation,
providing strong evidence that play and other social experiences (e.g., interacting
 How Play Makes for a More Adaptable Brain 89

with multiple partners) during the juvenile period are critical for refining the
neural circuits of the PFC that are involved in producing a socially competent
adult (Pellis, Pellis, and Bell 2010).
The PFC and several subcortical structures we believe to be involved in the
neural circuitry for executive function are activated during playful interactions
(Cheng, Taravosh-Lahn, and Delville 2008; Gordon et al. 2002). This includes
the amygdala, which is essential for the expression of emotion (van Kerkof et al.
2014). Given the play-induced structural changes in the neurons of the mPFC,
we could expect that the cells in the amygdala would also undergo structural
remodeling, but preliminary data suggest that this is not the case (Himmler,
unpublished observations). As noted previously, rats that are socially isolated and
so denied the opportunity to engage in playful interactions during the juvenile
period exhibit deficits in emotional regulation (e.g., da Silva et al. 1996; von
Frijtag et al. 2002). Therefore, it seems possible that the play-induced changes
in emotional regulation may arise from improved control of subcortical sys-
tems by neurons coming from the cortex, like those from the mPFC, that are
changed structurally by the experience of play. Because there are strong con-
nections between the mPFc and the subcortical neural systems that make up
the executive-control complex, the play-induced activation of both the cortical
and subcortical circuits may strengthen their connections. While this possibility
remains to be tested, closer consideration of the anatomical links between the
mPFC and selected subcortical circuits makes it a plausible hypothesis.
The mPFC has strong excitatory connections with multiple nuclei in the
amygdala, including the intercalated (ITC) and the basolateral nuclei (BLA). A
majority of the connections from both of these nuclei are then sent to the central
amygdala (CeA), which then projects to a variety of structures in the limbic system.
Whereas cells in the BLA are excitatory (McDonald et al. 1989), the cells in the
ITC are inhibitory (Nitecka and Ben-Ari 1987; McDonald and Augustine 1993;
Paré and Smith 1993). Therefore, information sent through the BLA (excitatory)
and the ITC (inhibitory) neurons are likely to have different effects on the target
systems. Given that mPFC has strong connections to both these nuclei in the
amygdala, some of the deficits seen in emotional regulation due to play depriva-
tion may arise from reduced regulatory control of the amygdala by the mPFC. In
part, the mPFC may exert regulatory control by modulating the activation of the
excitation and inhibition of the specific nuclei in the amygdala (Rosenkranz and
Grace 2002). Regardless of the specific mechanisms, the play-induced changes to
the mPFC likely have an effect on the regulation of the amygdala.
90 AMERICAN JOURNAL OF P L AY sFALL 2014

The dorsal raphe nuclei (DRN) constitute another subcortical area acti-
vated by playful interactions (van Kerkof et al. 2014). The majority of the neu-
rons that innervate the DRN come from the mPFC (Peyron et al. 1998; Vertes
2004), and these connections act to inhibit serotonin neurons (Jankowski and
Sesack 2004; Hajos et al. 1998). The DRN is strongly activated if animals encoun-
ter uncontrollable stress and this is coupled with heightened levels of fear and
anxiety (Grahan et al. 1999; Maswood et al. 1998). However, the strength of
this activation and behavioral response can be reduced if animals are exposed
to mild controllable stressors earlier in life. The attenuation of DRN activation
likely arises from improved regulatory control from the mPFC (Amat et al.
2005; Amat et al. 2006).
Linking these neural connections with play suggests the following model.
Engaging in playful interactions, young rats are exposed to both controllable
and uncontrollable situations (Pellis, Pellis, and Foroud 2005), and it is these
experiences that are hypothesized to influence the development of the mPFC
(Pellis, Pellis, and Bell 2010). In turn, these play-induced changes to the mPFC
may improve the regulatory control of the mPFC over subcortical regions such
as the amygdala and the DRN. These play-induced changes in neural organiza-
tion are the basis for the improved executive control present in rats that have
played as juveniles.

Conclusion

Why do rats have complex patterns of play fighting that contribute to the juve-
nile experiences that, in turn, refine the development of the neural circuits that
regulate executive function? And, why do mice not have these patterns of play?
Mice and rats have much of their behavioral repertoire in common, but for
a wide range of naturally occurring behaviors and in tasks requiring motor
and cognitive-skill acquisition, mice appear to be a pared-down version of rats
(Whishaw et al. 2001). Quite simply, mice have a behavioral repertoire that is
only modestly capable of being refined. Possibly, this results from mice having a
shorter life span and achieving sexual maturity at a younger age than do rats, so
that the capacity for excessive refinement of skills would be counterproductive—
i.e., the cost of such a capacity would exceed the benefit. For their part, rats live
in a somewhat more complex social system, have a longer lifespan, and reach
sexual maturity at a later age, increasing the benefits that arise from an increased
 How Play Makes for a More Adaptable Brain 91

capacity to be more flexible in dealing with unpredictable events (Whishaw et

al. 2001). There is support for such a hypothesis.
It has been shown that in rodents, primates, and birds more complex pat-
terns of play correlate with longer juvenile periods (Diamond and Bond 2003;
Pellis and Iwaniuk 2000b), and, in turn, longer juvenile periods are correlated
with larger brain sizes and a greater variety and flexibility in species typical
behavior (Joffe 1997; Walker et al. 2006). Moreover, innovative ability correlates
with increased brain size, especially in those brain areas associated with executive
function (Lefebvre, Reader, and Sol 2004; Reader and Laland 2002).
When comparing primate species, those that have more complex social
systems require more nuanced social cognition and actions, and these are the
species that are also more likely to use play in adulthood as a social tool for
assessment and manipulation (Pellis and Iwaniuk 2000a; Ciani et al. 2012; Palagi
2006). Importantly, with regard to the role of play in the juvenile period promot-
ing improved executive function, the juveniles of such species have a modified
pattern of play that exaggerates the experiences shown to be important for the
development of such capabilities (Reinhart et al. 2010). Indeed, these changes
in the pattern of play, such as increasing the movements that lead to loss of
control (Pellis, Pellis, and Foroud 2005), are associated with changes in factors
related to the timing of development—they extend the juvenile period (Palagi
and Cordoni 2012). These age-related changes in development, which lead to
longer juvenile periods and to the retention of more juvenile-like features into
adulthood, are the same kinds of processes that underlie domestication (Hare,
Wobber, and Wrangham 2012). Interestingly, domestication in rats has made
them more playful and more likely to engage in wrestling (Himmler et al. 2013),
whereas the play fighting of domesticated mice (Pellis and Pasztor 1999) is little
different from that of the wild type (Wolff 1981).
Thus, like other transformations in play (Burghardt 2005), there are likely
important enabling factors, such as an enlarged brain, a long juvenile period,
and complex social systems, that create the conditions that make it beneficial to
change the pattern of play to refine the brain’s executive functions. It is among
such species that we can find the role of play in making the brain more adaptable.

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