ADHD and Play

• Sheri Six, Washington State University, Pullman, WA, USA

• Dr. Jaak Panksepp, Washington State University, Pullman, WA, USA

ADHD: According to the Diagnostic and Statistical Manual of Mental Disorders (4th ed., text rev.; DSM-IV-TR; American Psychiatric Association, 2000), ADHD (Attention-Deficit/Hyperactivity Disorder), is a mental disorder characterized by inattention, hyperactivity and impulsivity at higher levels than typical for a given level of development. What causes ADHD is not completely known but magnetic resonance imaging (MRI) has shown that children with ADHD have slightly smaller brains, especially in frontal cortical areas (~5%) involved in executive functions (e.g., impulse control) and coordination of movements (Krain & Castellanos, 2006).

Children with ADHD often have difficulties in school due, at least in part, to an inability to sit still for long periods of time, to follow classroom rules, and to attend to assignments. In addition, their behavior may be off-putting to peers, possibly resulting in social rejection. Psychostimulants, such as methylphenidate, are commonly used to treat symptoms of ADHD but little is known about their long-term effect on children’s physical and mental development.

Play: Free play, in which children develop their own activities, including rough-and-tumble activities that, as the term play implies, involves physical activity such as running, jumping, play fighting, and wrestling, are increasingly recognized as essential components of a child’s development. Both human and animal studies have provided evidence that periods of play improve social skills, impulse inhibition and attention (Panksepp, 2007; Pellis et al., 2010) and result in specific neurochemical and dendritic changes in many neurons (Bell et al., 2010; Panksepp, 2008), especially in those brain areas in which ADHD children are deficient. Therefore, long-term provision of more opportunities for physical play may be an effective, non-medicinal therapy for reducing some of the disruptive behaviors of ADHD and facilitating brain development in children diagnosed with ADHD.

Indicators and Neuroanatomy of ADHD

It is commonly thought that, beside various environmental influences, the genesis of ADHD involves diverse gene expression patterns each with small individual effects (Tripp & Wickens, 2009). The visible indicators of ADHD, occurring either individually or in any combination, include most prominently the inability to maintain focus or attention for longer periods of time, hyperactivity and diminished impulse control. Children with ADHD may also exhibit aggressive behaviors, and hence be diagnosed with comorbid disorders such as Conduct Disorder and Oppositional Defiant Disorder.

Peer Relationships

As may be expected, children with ADHD have more difficulty with peer relationships than children without ADHD. In a study of 165 children (7-9 years) with ADHD, Hoza et al. (2005) found that these children had fewer friendships and were viewed negatively by peers. Indeed, 52% of the children studied fell into the rejected category based on measures of “social preference”, “social impact” and “liking”. Their lack of social success appears to be due, at least in part, to problems interpreting and responding to social cues. Andrade et al. (2012) found that, when compared with controls, children with ADHD and Conduct Problems i) tended to miss social cues (possibly due to inattention or working memory deficits), ii) interpret intentions of others and outcomes of interactions differently (both more positively or more negatively), and iii) often exhibit more negatively valenced responses to negative social situations (whereas, controls tended to exhibit more positive responses, even in negative situations). Thus, the social awkwardness, misinterpretations and mistakes made by children with ADHD often results in social neglect or outright rejection by peers, which obviously amplifies social problems.

The quality of friendships and peer relationships or lack thereof have long-term effects as children mature into adults. Childhood rejection by peers is predictive of negative behaviors (e.g., delinquency, substance abuse, dropping out of school, criminal activity) and feelings (e.g., depression, loneliness, anxiety (Parker and Asher, 1987; Rubin et al., 1998). However, it is important to remember that these results are not due to rejection alone; many other factors such as peer group choice come into play.

ADHD Endophenotypes

Castellanos and Tannock (2002) have identified three potential neuroscience-based endophenotypes that involve the executive functions of the brain. 1) Hyperactive behavior may be a result of a shortened delay gradient, which decreases the time one is willing to wait for a reward (e.g., recess, food treat, money, etc.). They hypothesize that fidgeting or hyperactivity may reflect a self-regulatory behavior when waiting is enforced. 2) Waiting, even for short times, may be extra difficult for people with ADHD because of differences in temporal processing that skew perceptions of time. Deficits in temporal processing may also be responsible for inattentive behaviors and inconsistent performance often seen in people with ADHD. 3) The final proposed endophenotype reflects a working memory deficit that affects executive functions (including impulse control), ability to maintain attention/focus, and even phonemic awareness deficits (e.g., dyslexia). Deficits in working memory may also promote the shortened reward-delay gradient that characterizes ADHD.

Neuroanatomy of ADHD

MRI monitored brain structural comparisons of children with ADHD and children without ADHA have produced conflicting results but some general conclusions can be made. In their review of recent studies, Krain and Castellanos (2006), report a 3.2-4% reduction in overall ADHD brain size, including especially reductions in the frontal, parietal, temporal and occipital lobes. However, differences in the frontal lobe, especially the prefrontal cortex (PFC), account for most of this reduction. Significant reductions have also been found in the cerebellum, an area involved in motor, timing, and attentional functions. Krain and Castellanos describe grey and white matter volume differences, both reductions and increases, in the PFC as well as many other brain areas. Variations have also been found in the size and asymmetry of the caudate nucleus and volume of the putamen but results are less consistent in these areas. It is important to note that some of these brain differences are found in young children but are no longer seen in adolescence (e.g., caudate volumes seem to normalize around age 16). It is generally believed that ADHD reflects deficits in brain dopamine transmission; solid evidence for that is lacking (Tripp & Wickens, 2009) but clearly dopamine influences need to be considered in the context of other brain neurochemical patterns (Oades, 2008). Thus, researchers have not been able to conclude that any of these brain variations are causal factors for ADHD behaviors, though neural correlations with response inhibition, impulsivity, hyperactivity, and attention have been found.

Cultural Attitudes of ADHD

Despite the differences found in neuroanatomy, there is disagreement regarding whether they constitute actual pathology or just natural variation. Many also question whether the prevalence of ADHD diagnoses accurately depicts a real disorder or if it is more indicative of cultural impatience with rambunctious children who do not conform to societal expectations of behavior (Panksepp, 1998a, 2007; Timimi and Taylor, 2004) or even the result of adults’ attempts to maintain the upper hand in adult-child power relationships (Jacobson, 2006).

There is indirect evidence that supports cultural influences on at least some ADHD diagnoses: Murrow and colleagues (2012) found that children in Canada who were born just prior to the annual cut-off date for school entry (i.e., youngest members of a given class) were more likely to be diagnosed with ADHD (30% for boys; 70% for girls) than those born just after the cut-off (i.e., oldest members of the class). Furthermore, these children were more likely to be prescribed medication treatment (41% for boys; 77% for girls). Similarly, when 473 child and adolescent psychotherapists in Germany were given a case vignette and asked to make a diagnosis, 16.7% diagnosed ADHD even when all diagnostic criteria were not met. This error in diagnosis occurred more often in case vignettes involving boys and, interestingly, was more likely to be made by male psychotherapists (Bruchmüller et al., 2012). This suggests that at least some diagnoses are based on cultural values, gender or children’s behavior relative to others rather than on rigorous attention to diagnostic criteria.

Play: A Primary-Process Emotional Circuit

Humans are born with a sophisticated brain that is ready to take in sensory information, to learn and to grow. However, we are not born with brains fully encoded and knowledgeable of the variety of experiences we may encounter throughout our lives. Instead, much of the higher brain can be considered to be “empty”—to be a tabula rasa—that is programmed by epigenetic effects that are modulated by developmental experiences (Meaney, 2012). However, genetically ingrained tools for living clearly exist in subcortical brain regions. Functional evidence indicates that our brains contain at least seven primary-process emotional systems, shared by all mammals, that help us anticipate and respond to situations that promote or threaten our survival (Panksepp, 1998b; Panksepp & Biven, 2012). These systems compel mammals to explore, to fear dangerous situations and to care for young. They also drive mammals, especially the young, to play.

The details of the play circuitry are not fully known but lesions to the parafascicular complex and posterior dorsomedial thalamic nuclei reduce play behaviors in rats, strongly suggesting that these areas make up part of the play circuit (Panksepp, 1998b; Panksepp & Biven, 2012). Other brain areas that may be involved include the cerebellum, basal ganglia, and various hypothalamic areas but many of these areas are also involved in movement or aggression, both of which could affect one’s desire or ability to play. Neocortex, however, is not directly involved in play. Decorticated juvenile rats (neocortex ablated in infancy) show a normal desire to play but with some modest differences in the number and duration of play behaviors. However, these differences disappear when playing with non-decorticated play partners (Panksepp et al., 1994).

Taken together, the evidence supports the assertion that play is one of the primary-process brain circuits, devised through evolution, that promote instinctual feelings and behaviors, and ultimately aid development of the mature social brain.

Benefits of Play

The human brain develops rapidly during the first two years of life after which neuronal growth, cortical organization and refinement of synapses continues at a slower pace into adulthood (see review by Halperin & Healey, 2011). Play has been found to effect significant changes in the brain and is likely, therefore, an important factor in brain development. Dendritic length, complexity and spine density of the medial prefrontal cortex (mPFC) are refined by play. The orbitofrontal cortex also changes but its increases in dendritic length and complexity are due to the effect of multiple social partners rather than play itself (Bell et al., 2010; Pellis et al., 2010). In addition, play increases neuronal growth promoting BDNF mRNA in amygdala and dorsolateral frontal cortex (Gordon et al., 2003) and insulin like growth factor I (IGF-I), which is associated with positive affect (Burgdorf et al., 2010), and modifies many other genes in the cortex (Moskal, et al., 2011).

Though the specific functional effects of these changes are not yet understood, researchers have shown direct behavioral effects of play on ADHD type symptoms in animals. Panksepp and colleagues (2003) found that play in rats reduced hyperactivity and possibly promoted behavioral inhibition and attention to surroundings, all of which are likely factors affecting children’s academic and social success. Significant social effects were reviewed by Pellis, Pellis and Bell (2010) in which rats without play were found to have difficulties socializing with other rats due to inappropriate social behaviors, lack of emotional control, hyperdefensiveness, elevated susceptibility to stress, and a decreased ability to accurately predict and respond to the movements of social partners. Thus, though play may not be necessary for brain maturation, it appears to be vital to the development of social skills and self-control (see Figure 1).

Research into the benefits of play is only just beginning but results suggest that adding ample play opportunities may help improve the success of ADHD treatment, especially in regards to social success, which thus far has been little improved by stimulant or behavioral treatments (King et al., 2009; Mrug et al., 2012). We must keep in mind, though, that children with ADHD often have difficulties making and keeping friends (Hoza, 2007; Hoza et al., 2005; Andrade et al., 2012), probably due to poor social skills, and their play can often end in aggression and rejection (Panksepp & Scott, 2012) so many play interactions may result in negative rather than positive experiences. One way to minimize the number of negative play outcomes may be to provide children with abundant rough and tumble play experiences that build and refine the social brain during the first few years of children’s lives before any ADHD diagnosis is appropriate. Play, after all, is beneficial for all children, not just children with ADHD. Since play also improves self-control, attention and hyperactivity, it may be that early play could prevent at least some diagnoses of ADHD as children age.

Risks of Psychostimulant Treatment

Psychostimulants, usually methylphenidate (MPH), are common first line treatments for ADHD (De Sousa and Kalra, 2012), especially in the United States, which has one of the highest rates of MPH consumption (INCB, 2012). These drugs tend to effectively improve attention, focus and some academic achievement and to reduce some inappropriate behaviors (De Sousa and Kalra, 2012). However, in their review of long-term studies, Swanson et al. (2011) noted that psychostimulants were more effective for non-executive cognitive functions and less so for executive tasks. Over all, they report that some follow-up studies have found that adults benefitted from taking stimulant medication in childhood, though these participants were self-selected so the results may not be generalized to the whole population.

There are many physiological concerns regarding stimulant use for children. Common side effects are reduced appetite, weight loss, increased heart rate, and retarded growth. Other side effects include insomnia, headaches, nervousness, irritability, dizziness, anorexia, nausea, seizures, hallucinations and worsening of tics, which may affect children’s quality of life and mental state (De Sousa and Kalra, 2012; Urban and Gao, 2012). Furthermore, stimulants have long been known to decrease play (Panksepp, 2007), which, as mentioned above, is an important factor in brain development.

Brain development may also be immediately and, perhaps, permanently affected by stimulant use. In their review of the literature, Urban and Gao (2012) found that MPH use during the juvenile period resulted in long-term neurochemical and neuroanatomical brain changes that may last throughout life. Stimulant use has also been associated with changes in brain plasticity that may contribute to addiction (Robinson and Kolb, 2004), though adolescents with untreated ADHD may also be more likely to have substance use disorders (Wilens and Biederman, 2006). There is serious concern that MPH use may sensitize children to drugs and thereby promote addiction in adolescents and adults, but to date, evidence on these point remains inconclusive (Panksepp, 2007). To some indeterminate extent, the mixed results are probably due to individual differences in ADHD children and diverse procedural differences in animal studies (Gill et al., 2012).

Given the known side effects of stimulants and the lack of knowledge regarding their immediate and long-term brain effects, more targeted research is required. In the meantime, caution should be used when determining whether to medicate ADHD children, perhaps with an emphasis on non-drug interventions such as play before moving to medication as a last resort. Indeed, it is best that children have a regular “diet” of play from their earliest years, with enough adult supervision to assure that naughty behaviors can be discouraged, and hence the positive benefits of play can be consolidated into lasting adaptive behavior patterns, characterized by good self-regulation and empathy toward others. As Plato said over two millennia ago: “Our children from their earliest years must take part in all the more lawful forms of play, for if they are not surrounded with such an atmosphere they can never grow up to be well conducted and virtuous citizens” (The Laws [VII, 794]).

References

• Andrade, B. F., Waschbusch, D. A., Doucet, A., King, S., MacKinnon, M., McGrath, P. J., Stewart, S. H., & Corkum, P. (2012). Social information processing of positive and negative hypothetical events in children with ADHD and Conduct Problems and Controls. Journal of Attention Disorders, 16(6), 491-504.
• American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed., text rev.). doi:10.1176/appi.books.9780890423349.
• Bell, H. C., Pellis, S. M. & Kolb, B. (2010). Juvenile peer play experience and the development of the orbitofrontal and medial prefrontal cortices. Behavioural Brain Research, 207, 7-13.
• Bruchmüller, K., Margraf, J., & Schneider, S. (2012). Is ADHD diagnosed in accord with diagnostic criteria? Overdiagnosis and influence of client gender on diagnosis. Journal of Consulting and Clinical Psychology, 80, 128-138.
• Burgdorf, J., Kroes, R. A., Beinfeld, M. C., Panksepp, J., & Moskal, J. R. (2010). Uncovering the molecular basis of positive affect using rough-and-tumble play in rats: A role for insulin-like growth factor I. Neuroscience, 168, 769-777.
• Castellanos, F. X., & Tannock, R. (2002). Neuroscience of attention-Deficit/Hyperactivity Disorder: The search for endophenotypes. Nature Reviews. Neuroscience, 3, 617-628.
• Coppens, C. M., Siripornmongcolchai, T., Wibrand, K., Alme, M. N., Buwalda, B. de Boer, S. F., Koolhaas, J. M., Bramham, C. R. (2011). Social defeat during adolescence and adulthood differentially induce BDNF-regulated immediate early genes. Frontiers in Behavioral Neuroscience, 5, 1-8.
• De Sousa, A., & Kalra, G. (2012). Drug therapy of attention deficit hyperactivity disorder: Current trends. Mens Sana Monographs, 10, 45-69.
• Dodge, K. A., Pettit, G. S., McClaskey, C. L., Brown, M. M., & Gottman, J. M. (1986). Social competence in children. Monographs of the Society for Research in Child Development, 51(2, Serial No. 213), i+iii+v-vi+1-85.
• Gill, K. E., Pierre, P. J., Daunais, J., Bennett, A. J., Martelle, S.,...Porrino, L. J. (2012). Chronic treatment with extended release methylphenidate does not alter dopamine systems or increase vulnerability for cocaine self-administration: A study in nonhuman primates. Neuropsychopharmacology, Epub ahead of print, July 18, 2012. DOI: 10.1038/npp.2012.117
• 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.
• Halperin, J. M., & Healey, D. M. (2011). The influences of environmental enrichment, cognitive enhancement, and physical exercise on brain development: Can we alter the developmental trajectory of ADHD? Neuroscience and Biobehavioral Review, 35, 621-634.
• Hoza, B. (2007). Peer functioning in children with ADHD. Journal of Pediatric Psychology, 32, 655-663.
• Hoza, B., Mrug, S., Gerdes, A. C., Hinshaw, S. P., Bukowski, W. M., Gold, J. A., Kraemer, H. C., Pelham, W. E. Jr., Wigal, T., Arnold, L. E. (2005). What aspects of peer relationships are impaired in children with attention-deficit/hyperactivity disorder? Journal of Consulting and Clinical Psychology, 73, 411-423.
• International Narcotics Control Board. (2012). Psychotropic substances. Statistics for 2010 Assessments of annual medical and scientific requirements for substances in Schedules II, III and IV of the Convention on Psychotropic Substances of 1971. Ney York: United Nations Publications.
• Jacobson, K. (2006). ADHD from a cross-cultural perspective. Insights into adult-child power relationships. In Lloyd, G., Stead, J., & Cohen, D. (Eds.). Critical new perspectives on ADHD. New York, NY: Routledge.
• King, S., Waschbusch, D. A., Pelham, W. E., Jr., Frankland, B. W., Andrade, B. F., Jacques, S., & Corkum, P. V. (2009). Social information processing in elementary-school aged children with ADHD: medication effects and comparisons with typical children. Journal of Abnormal Child Psychology, 37, 579-589.
• Krain, A. L., & Castellanos, F. X. Brain development and ADHD. Clinical Psychology Review, 26, 433-444.
• Meaney, M. (2012). Epigenetics and the environmental regulation of the genome and its function. In Narvaez, D., Panksepp, J., Schore, A.N. & Gleason, T. (Eds). Evolution, early experience and human development: From research to practice and policy. New York: Oxford University Press.
• Moskal, J. R., Burgdorf, J., Kroes, R. A., Brudzynski, S. M., & Panksepp, J. (2011). A novel NMDA receptor glycine-site partial agonist, GLYX-13, has therapeutic potential for the treatment of autism. Neuroscience & Biobehavioral Reviews, 35, 1982-1988.
• Mrug, S., Molina, B. S. G., Hoza, B. Gerdes, A. C., Hinshaw, S P., Hechtman, L., Arnold, L. E. (2012). Peer rejection and friendships in children with attention-deficit hyperactivity disorder: Contributions to long-term outcomes. Journal of Abnormal Child Psychology, 40, 1013-1026.
• Murrow, R. L., Garland, E. J., Wright, J. M., Maclure, M. Taylor, S., & Dormuth, C. R. (2012). Influence of relative age on diagnosis and treatment of attention-deficit/hyperactivity disorder in children. Canadian Medical Association Journal, 184, 755-762.
• Oades, R. D. (2008). Dopamine-serotonin interactions in attention-deficit hyperactivity disorder (ADHD). Progress in Brain Research, 172, 543-565.
• Panksepp, J., Normansell, L., Cox, J. F., & Siviy, S. M. (1994). Effects of neonatal decortication on the social play of juvenile rats. Physiology & Behavior, 56, 429-443.
• Panksepp, J. (1998a). A critical analysis of ADHD, psychostimulants, and intolerance of childhood playfulness: A tragedy in the making? Current Directions in Psychological Sciences. 7, 91-97.
• Panksepp, J. (1998b). Affective neuroscience: The foundations of human and animal emotions. New York: Oxford University Press.
• Panksepp, J. (2007). Can PLAY diminish ADHD and facilitate the construction of the social brain? Journal of the Canadian Academy of Child and Adolescent Psychiatry, 16, 57-66.
• Panksepp, J. (2008). Play, ADHD, and the construction of the social brain. Should the first class of each day be recess? American Journal of Play, 1, 57-81.
• Panksepp, J., & Biven, L. (2012). The archaeology of mind: Neuroevolutionary origins of human emotion: Norton, W. W. & Company, Inc.
• Panksepp, J. & Scott, E. L. (2012). Reflections on rough and tumble play, social development, and attention-deficit hyperactivity disorders. In A. L. Meyer & T. P. Gullotta (Eds.)., Physical activity across the lifespan: Prevention and treatment for health and well-being (pp. 23-40). New York: Springer.
• Parker, J. G. & Asher, S. R. (1987). Peer relations and later personal adjustment: Are low-accepted children at risk? Psychological Bulletin, 102, 357-389.
• Pellis, S. M., Pellis, V. C., & Bell, H. C. (2010). The function of play in the development of the social brain. American Journal of Play, 2, 278-296.
• Robinson, T. E. & Kolb, B. (2004). Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology, 47, 33-46.
• Rubin, K. H., Bukowski, W., & Parker, J. G. (1998). Peer interactions, relationships and groups. In N. Eisenberg (Ed.)., Handbook of child psychology, Vol. 3, Social, Emotional and Personality Development (pp., 619-700). New York: Wiley.
• Swanson, J., Baler, R. D., & Volkow, N. D. (2011). Understanding the effects of stimulant medications and cognition in individuals with attention-deficit hyperactivity disorder: A decade of progress. Neuropsychopharmacology Reviews, 36, 207-226.
• Timimi, S., & Taylor, E. (2004). ADHD is best understood as a cultural construct. The British Journal of Psychiatry, 184, 8-9.
• Tripp, G. & Wickens, J.R. (2009). Neurobiology of ADHD. Neuropharmacology, 57, 579-589.
• Urban, K. R., & Gao, W.-J. (2012). Evolution of the study of methylphenidate and its actions on the adult versus juvenile brain. Journal of Attention Disorders, E-pub ahead of print, Aug 24, 2012. DOI: 10.1177/1087054712455504
• Wilens, T. E., & Biederman, J. (2006). Alcohol, drugs, and attention-deficit/hyperactivity disorder: A model for the study of addictions in youth. Journal of Psychopharmacology, 20, 580-588.

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

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

Reviewed by: Dr. Stuart L. Brown, National Institute for Play, Carmel Valley, CA, USA

Reviewed by: Dr. Scott Eberle, The Strong, Rochester, NY, USA

Accepted on: 2012-09-20 21:28:03 GMT