Social play in juvenile rats: A decade of methodological and experimental research

The social play behavior of juvenile rats was originally described nearly a century ago, but research methods have only recently included the controlled laboratory investigation of psychobiological variables. This review covers the experimental literature of social play or play fighting behavior in juvenile laboratory rats reported during the last decade. Innovative measures for quantifying social play are described; hormonal, pharmacological, and neurological variables are examined; and interpretative concepts of social play are discussed. The current emphasis on measures and procedures as well as the limited scope of current research effort suggests a formative stage of research development.     

Social play alters regional brain opioid receptor binding in juvenile rats

An in vivo autoradiographic procedure was employed to visualize local changes in brain opioid receptor occupancy in juvenile rats. This procedure is based on the assumption that released endogenous ligand will exclude exogenously applied tracer, in this case [³H]diprenorphine, from opioid receptors. Increases in availability of opioid peptides will then result in decreased opioid receptor binding. From behavioral studies there is ample evidence that opioid systems are involved in the regulation of social play behavior in juvenile rats. In the present study, changes in regional brain opioid activity as a result of social isolation-induced social play behavior were monitored. Twenty-one-day-old rats were socially isolated for 0, 3.5 or 24 h prior to testing, and tested alone or in a dyadic encounter. After behavioral testing, [³H]diprenorphine was administered and the brain was prepared for autoradiography. Social isolation caused increases in social behavior (dyadic encounters) but not in non-social behavior (singly tested animals). Modest differences in brain opioid receptor binding due to social isolation, social play behavior, or an interaction of the two, were found in claustrum, nucleus accumbens, globus pallidus, paraventricular and arcuate nuclei of the hypothalamus, and the dorsolateral and paratenial thalamic nuclei. These results support the notion that opioid systems are involved in the regulation of social play behavior. In addition, the observation of changes in opioid binding in areas involved in reward processes, adds evidence to the hypothesis that opioid systems are involved in the regulation of the rewarding aspects of social plah in juvenile rats.     

Early exposure to a low dose of bisphenol A affects socio-sexual behavior of juvenile female rats

Play behavior is affected by alteration of the hormonal environment during development. In fact, congenital adrenal hyperplasia or early administration of diethylstilbestrol are able to modify female play behavior in mammals. In this research, play behavior of female rats was used to explore the effects of perinatal exposure to low, environmentally relevant dose of bisphenol A (BPA), a xenoestrogen widely diffused in the environment. We used 18 females born to mothers exposed to 40 microg/kg/day BPA during pregnancy and lactation, and 18 control females. The subjects were observed in a heterosexual social situation from 35 to 55 days of age. Six main behaviors were identified by principal component analysis (PCA): exploration, defensive behavior to males, play behavior with males, play behavior with females, low-intensity mating behavior, social grooming. Early administration of BPA was responsible for a significant increase of exploration (including social investigation) (p<0.001), as well as a decrease of play with males (p<0.02) and social grooming (p<0.01) at 45 days of age, indicating a general decrease of playful interactions. In general our results suggest that BPA does not induce a clear masculinization of female behavior, but is able however to defeminize some aspects of female behavior. This result is compatible with the estrogenic properties of BPA, and suggests caution in the use of a chemical that, in the range of human exposure, is able to influence the development of the brain during a critical period, resulting in long-term effects on behavior.     

Developmental brain injury associated with abnormal play behavior in neonatally Borna disease virus-infected Lewis rats: a model of autism

Play behavior, nonsocial exploratory activity, and nonplay social interaction were observed in male juvenile Lewis rats with brain developmental injury following neonatal infection with Borna disease virus (BDV). These behaviors were tested using the ‘intruder-resident' paradigm, with social isolation of residents for six days prior to testing. Four experimental pairings of infected (BDV) and uninfected (NL) rats were studied as follows: NL–NL; NL–BDV; BDV–NL; and BDV–BDV (the first member is the resident, the second member is the intruder). Observation of social activities was carried out for 10 min on two consecutive days. Nonsocial exploratory activity (e.g. ambulation and rearing) was similar in BDV and NL residents. Duration of nonplay social investigation (e.g. sniffing, approach, and follow) was higher in BDV residents as compared to NL residents when tested on the first test day. On the second day, all rats showed similar level of nonplay social interaction. When confronted with NL intruders, NL residents exhibited significantly more play behavior compared to the NL–BDV, BDV–NL and BDV–BDV pairs, when play behavior was measured by the number of ‘pins'. Moreover, irrespective of a type of intruder, NL residents demonstrated higher play soliciting behavior than BDV residents, indicating attenuated readiness to play in BDV-infected rats. The number of pins and play solicitations in BDV–NL pairs significantly increased over the two days of testing, while play activity in NL–BDV pairs declined on the second test day. This pattern suggests that the degree of social reinforcement on the first day of testing affected the level of play on the second day. These data demonstrate deficits in play behavior and other social interactions following BDV-associated developmental brain injury, thus supporting the value of the neonatally BDV-infected rat as an animal model of autism.     

Social play development in pre-weaning olfactory deprived or stimulated rats

The effect of neonatal unilateral restriction or increased olfactory stimulation upon the development of social play behavior in Wistar strain rats was investigated. Pups were unilaterally thermocauterized in one of the nares on postnatal day 3 (experiment 1), or exposed to amyl acetate from 3 to 19 days of age (experiment 2). Unilateral odor deprivation significantly increased the frequency of boxing, wrestling and pinning in rats of both sexes. However, amyl acetate exposure significantly decreased the frequency of wrestling and pinning in females with no effects in males. The alterations in the development of social play behavior are concurrent with gross physical olfactory bulb modifications that may reflect a significant interference with the integration and transmission of olfactory stimuli to central structures such as septal, entorhinal, cingulate and midline frontal cortices subserving social play behavior. Data suggest that early in life brain mechanisms underlying social play behavior are sensitive to manipulation of neonatal olfactory cues and may participate in the modulation of this behavior.     

Use of LEGO© as a Therapeutic Medium for Improving Social Competence

A repeated-measures, waiting list control design was used to assess efficacy of a social skills intervention for autistic spectrum children focused on individual and group LEGO© play. The intervention combined aspects of behavior therapy, peer modeling and naturalistic communication strategies. Close interaction and joint attention to task play an important role in both group and individual therapy activities. The goal of treatment was to improve social competence (SC) which was construed as reflecting three components: (1) motivation to initiate social contact with peers; (2) ability to sustain interaction with peers for a period of time; and (3) overcoming autistic symptoms of aloofness and rigidity. Measures for the first two variables were based on observation of subjects in unstructured situations with peers; and the third variable was assessed using a structured rating scale, the SI subscale of the GARS. Results revealed significant improvement on all three measures at both 12 and 24 weeks with no evidence of gains during the waiting list period. No gender differences were found on outcome, and age of clients was not correlated with outcome. LEGO© play appears to be a particularly effective medium for social skills intervention, and other researchers and clinicians are encouraged to attempt replication of this work, as well as to explore use of LEGO© in other methodologies, or with different clinical populations.     

Social Stories: Mechanisms of Effectiveness in Increasing Game Play Skills in Children Diagnosed with Autism Spectrum Disorder Using a Pretest Posttest Repeated Measures Randomized Control Group Design

An increasing body of literature has indicated that social stories are an effective way to teach individuals diagnosed with autism appropriate social behavior. This study compared two formats of a social story targeting the improvement of social skills during game play using a pretest posttest repeated measures randomized control group design. A total of 45 children diagnosed with Autism Spectrum Disorder (ASD) ages 7–14 were randomly assigned to standard, directive, or control story conditions. Results demonstrated that the standard and directive story formats were equally as effective in eliciting, generalizing and maintaining the targeted social skills in participants who had prior game play experience and Verbal Comprehension Index (VCI) scores from the WISC-IV intelligence test in the borderline range or above.     

Morphine treatment during juvenile isolation increases social activity and opioid peptides release in the adult rat

The consequences of juvenile isolation and morphine treatment on general activity, social activity and endogenous opioid release during a social interaction test were investigated in the adult rat. Rats were either isolated or socially housed during weeks 4 and 5 of age and treated daily during this isolation period subcutaneously with either saline or morphine. Directly after a social interaction test at 10 weeks of age, rats were injected with [3H]-diprenorphine and subsequently prepared for in vivo autoradiography. The autoradiographic technique was used to visualise neuroanatomical changes in opioid receptor occupancy, probably reflecting changes in opioid peptide release, as a result of social activity. Juvenile isolation increased general activity during the social interaction test, an effect which was accompanied by a reduction of opioid receptor occupancy in many brain areas, suggesting an increased opioid peptide release as a consequence of socially-induced general activity. Morphine treatment in isolated rats caused an increase in adult social activity and enhanced opioid peptide release in some cortical regions and the ventral tegmental area as compared to saline treated rats. Both social activity and opioid receptor occupancy were unaffected by morphine treatment in non-isolated rats. The present study underscores the role of opioid systems in adult social behaviors as a consequence of juvenile isolation. The results suggest a relationship between social activity and opioid peptide release during social contact. Increased social activity seems to be accompanied by elevated opioid peptide release in distinct brain areas after morphine treatment during juvenile isolation.     

Examining the relationship between social communication on the ADOS and real-world reciprocal social communication in children with ASD

BackgroundWhile many children with autism spectrum disorders (ASDs) communicate better with adults than peers, diagnostic measures are given by adult examiners. These measures may not accurately capture the deficits that children with ASD have in communicating with their peers.MethodThis study examined the ability of the Autism Diagnostic Observation Schedule (ADOS) Social Communication scale to predict reciprocal communication in children with ASD during natural play with peers using the Peer Interaction Paradigm (PIP). Thirty participants with ASD were given the ADOS and then participated in the PIP, after which their behavior was analyzed.ResultsUsing linear regression, we found that Social Communication was the primary significant predictor for reciprocal communication during play, and that reciprocal communication was not predicted by Verbal IQ or the Restrictive and Repetitive Behaviors scale on the ADOS.ConclusionsThe findings suggest that the ADOS measures naturally-occurring social communication patterns with peers and can be used to inform treatment options for children with ASD based on an accurate measure of their level of impairment in social communication.