The Function of Play in the Development of the Social Brain.

Rough-and-tumble play, or play fighting, is common in the young of many mammals. Research on play fighting among rats shows that there are many levels of neural control over this behavior: subcortical mechanisms mediate the motivation and behavior of such play, and the cortex provides mechanisms by which the play changes with age and context. The cortical mechanisms help to explain the advantages playing offers the brain. The cortically induced modulations of the content of play with age ensure that exposure to particular kinds of experiences are enhanced during the critical juvenile period. These experiences, in turn, modify the development of other areas of the cortex. Such cortical changes appear to mediate the effects of play on the refinement of social skills. As a result, rats that play as juveniles are more socially competent as adults. This work was supported by the Natural Sciences and Engineering Research Council of Canada and the Alberta Heritage Foundation for Medical Research.

[1]  Stanley J. Watson,et al.  Socially-induced brain ‘fertilization’: play promotes brain derived neurotrophic factor transcription in the amygdala and dorsolateral frontal cortex in juvenile rats , 2003, Neuroscience Letters.

[2]  B. McEwen,et al.  Stress and cognitive function , 1995, Current Opinion in Neurobiology.

[3]  M. Morgan,et al.  A critical period for social isolation in the rat. , 1977, Developmental psychobiology.

[4]  B. M. Spruijt,et al.  Isolation during the play period in infancy decreases adult social interactions in rats , 1999, Behavioural Brain Research.

[5]  S. Pellis,et al.  Attack and Defense During Play Fighting Appear to be Motivationally Independent Behaviors in Muroid Rodents , 1991 .

[6]  G. Metz,et al.  Dietary restriction alters fine motor function in rats , 2005, Physiology & Behavior.

[7]  R. Bolles,et al.  The ontogeny of behaviour in the albino rat , 1964 .

[8]  T. Caro,et al.  On the Functions of Play and Its Role in Behavioral Development , 1985 .

[9]  S. Pellis,et al.  Some subordinates are more equal than others: Play fihgting amongst adult subordinate male rats , 1993, Aggressive Behavior.

[10]  E. Palagi Social play in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): Implications for natural social systems and interindividual relationships. , 2006, American journal of physical anthropology.

[11]  A. Brownlee Play in Domestic Cattle in Britain: An Analysis of its Nature , 1954, Nature.

[12]  S. Pellis,et al.  The developmental onset of a rudimentary form of play fighting in C57 mice. , 1999, Developmental psychobiology.

[13]  S. Pellis,et al.  The effects of orbital frontal cortex damage on the modulation of defensive responses by rats in playful and nonplayful social contexts. , 2006, Behavioral neuroscience.

[14]  S. Pellis,et al.  Adult–Adult Play in Primates: Comparative Analyses of its Origin, Distribution and Evolution , 2000 .

[15]  Euclid O. Smith A HISTORICAL VIEW ON THE STUDY OF PLAY STATEMENT OF THE PROBLEM1 , 1978 .

[16]  G. Burghardt The Genesis of Animal Play: Testing the Limits , 2005 .

[17]  S. Siviy Animal Play: Neurobiological sustrates of play behavior: glimpses into the structure and function of mammalian playfulness , 1998 .

[18]  M. Schwab,et al.  The effects of acute and chronic stress on motor and sensory performance in male Lewis rats , 2001, Physiology & Behavior.

[19]  S. Pellis Exploration and Play in the Behavioural Development of the Australian Magpie Gymnorhina tibicen , 1981 .

[20]  S. Pellis,et al.  Rough-and-Tumble Play and the Development of the Social Brain , 2007 .

[21]  R. Fagen Animal Play Behavior , 1981 .

[22]  A. Walf,et al.  The use of the elevated plus maze as an assay of anxiety-related behavior in rodents , 2007, Nature Protocols.

[23]  Julie A. Markham,et al.  Neuron number decreases in the rat ventral, but not dorsal, medial prefrontal cortex between adolescence and adulthood , 2007, Neuroscience.

[24]  Head rotations in the play of Hanuman langurs (Semnopithecus entellus): description and analysis of function. , 2008, Journal of comparative psychology.

[25]  S. Pellis,et al.  The development of a sex-differentiated defensive motor pattern in rats: A possible role for juvenile experience. , 1999, Developmental psychobiology.

[26]  J. Baldwin,et al.  Exploration and Social Play in Squirrel Monkeys (Saimiri) , 1974 .

[27]  S. Pellis,et al.  Play and the Development of Social Engagement: A Comparative Perspective. , 2006 .

[28]  M. Špinka,et al.  Mammalian Play: Training for the Unexpected , 2001, The Quarterly Review of Biology.

[29]  R. van den Bos,et al.  Individual housing during the play period results in changed responses to and consequences of a psychosocial stress situation in rats. , 2002, Developmental psychobiology.

[30]  J. Fuster Prefrontal Cortex , 2018 .

[31]  S. Pellis,et al.  The role of the medial prefrontal cortex in the play fighting of rats. , 2009, Behavioral neuroscience.

[32]  L. Vanderschuren,et al.  The neurobiology of social play behavior in rats , 1997, Neuroscience & Biobehavioral Reviews.

[33]  J. Panksepp The ontogeny of play in rats. , 1981, Developmental psychobiology.

[34]  J. Panksepp,et al.  Effects of neonatal decortication on the social play of juvenile rats , 1994, Physiology & Behavior.

[35]  A. Carobrez,et al.  Individual Housing From Rearing Modifies the Performance of Young Rats on the Elevated Plus-Maze Apparatus , 1996, Physiology & Behavior.

[36]  S. Pellis,et al.  Evolving a Playful Brain: A Levels of Control Approach , 2004 .

[37]  Jack A. Naglieri,et al.  Exercise and Children’s Intelligence, Cognition, and Academic Achievement , 2008, Educational psychology review.

[38]  S. Pellis,et al.  Play Fighting: Aggression, Affiliation, and the Development of Nuanced Social Skills. , 2005 .

[39]  Environmental influences on play behaviour in immature gelada baboons , 1992, Animal Behaviour.

[40]  M. Potegal,et al.  Aggressive behaviors in adult rats deprived of playfighting experience as juveniles. , 1989, Developmental psychobiology.

[41]  Benno Roozendaal,et al.  Stress and Memory: Opposing Effects of Glucocorticoids on Memory Consolidation and Memory Retrieval , 2002, Neurobiology of Learning and Memory.

[42]  S. Pellis,et al.  The role of the cortex in play fighting by rats: developmental and evolutionary implications. , 1992, Brain, behavior and evolution.

[43]  S. Pellis,et al.  Development of “Anchoring” in the Play Fighting of Rats: Evidence for an Adaptive Age-Reversal in the Juvenile Phase , 2002, International Journal of Comparative Psychology.

[44]  S. Pellis,et al.  Juvenile peer play experience and the development of the orbitofrontal and medial prefrontal cortices , 2010, Behavioural Brain Research.

[45]  M. Morgan,et al.  Brief periods of socialization and later behavior in the rat. , 1978, Developmental psychobiology.

[46]  D. H. Thor,et al.  Play-solicitation behavior in juvenile male and female rats , 1983 .

[47]  H. Arakawa The effects of isolation rearing on open-field behavior in male rats depends on developmental stages. , 2003, Developmental psychobiology.

[48]  S. Paradiso The Emotional Brain: The Mysterious Underpinnings of Emotional Life , 1998 .

[49]  S. Pellis,et al.  Play‐fighting differs from serious fighting in both target of attack and tactics of fighting in the laboratory rat Rattus norvegicus , 1987 .

[50]  A. Stone Seasonal Effects on Play Behavior in Immature Saimiri sciureus in Eastern Amazonia , 2008, International Journal of Primatology.

[51]  D. H. Thor,et al.  Developmental analyses of social play behavior in juvenile rats , 1984 .

[52]  T. Robinson,et al.  Plasticity and functions of the orbital frontal cortex , 2004, Brain and Cognition.

[53]  E. Palagi,et al.  Immediate and Delayed Benefits of Play Behaviour: New Evidence from Chimpanzees (Pan troglodytes) , 2004 .

[54]  J. Byers,et al.  Refining the Motor Training Hypothesis for the Evolution of Play , 1995, The American Naturalist.

[55]  Sergio M Pellis,et al.  Experience and cortical control over the pubertal transition to rougher play fighting in rats , 2004, Behavioural Brain Research.

[56]  J. Koolhaas,et al.  Play is indispensable for an adequate development of coping with social challenges in the rat. , 1999, Developmental psychobiology.

[57]  J. Berger Social ontogeny and behavioural diversity: consequences for Bighorn sheep Oris canadensis inhabiting desert and mountain environments , 2009 .

[58]  S. Pellis Sex Differences in Play Fighting Revisited: Traditional and Nontraditional Mechanisms of Sexual Differentiation in Rats , 2002, Archives of sexual behavior.

[59]  John Alcock Animal behavior: An evolutionary approach, 4th ed. , 1989 .

[60]  J. Panksepp Affective Neuroscience: The Foundations of Human and Animal Emotions , 1998 .

[61]  M. Potegal,et al.  Enhanced defense in adult rats deprived of playfighting experience as juveniles , 1991 .

[62]  S. Pellis,et al.  The modulation of play fighting in rats: role of the motor cortex. , 2007, Behavioral neuroscience.

[63]  B. Kolb,et al.  The Cerebral cortex of the rat , 1990 .

[64]  J. Panksepp,et al.  Sensory modulation of juvenile play in rats. , 1987, Developmental psychobiology.

[65]  S. Pellis,et al.  Mechanisms underlying the absence of the pubertal shift in the playful defense of female rats. , 1998, Developmental psychobiology.

[66]  G. Metz,et al.  Modulation of motor function by stress: a novel concept of the effects of stress and corticosterone on behavior , 2005, The European journal of neuroscience.