A Brain Motivated to Play: Insights into the Neurobiology of Playfulness

Play is an important part of normal childhood development and is seen in varied forms among many mammals. While not indispensable to normal development, playful social experiences as juveniles may provide an opportunity to develop flexible behavioural strategies when novel and uncertain situations arise as an adult. To understand the neurobiological mechanisms responsible for play and how the functions of play may relate to these neural substrates, the rat has become the model of choice. Play in the rat is easily quantified, tightly regulated, and can be modulated by genetic factors and postnatal experiences. Brain areas most likely to be involved in the modulation of play include regions within the prefrontal cortex, dorsal and ventral striatum, some regions of the amygdala, and habenula. This paper discusses what we currently know about the neurobiological substrates of play and how this can help illuminate functional questions about the putative benefits of play

Effects of Neonatal Handling on Play Behavior and Fear Towards a Predator Odor in Juvenile Rats

The effects of brief daily separation, also known as handling, during the first 2 weeks of life on play behavior and fearfulness toward a predatory odor were assessed in juvenile rats. Handled rats were more playful than nonhandled control rats, and while handling had no effect on the direct response of these rats toward a predatory odor, handled rats did not exhibit a conditioned suppression of play when tested later in the same context where they had been exposed to the predatory odor. Handled rats were still wary of the environment in that they continued to show a heightened level of risk assessment behavior. These data suggest that early postnatal experiences may play a significant role in determining how an animal deals with predatory threats later in life

Play and Adversity: How the Playful Mammalian Brain Withstands Threats and Anxieties

Most mammals play, but they do so in a dangerous world. The dynamic relationship between the stresses created by their world and the activity of play helps to explain the evolution of play in mammals, as the author demonstrates in evidence garnered from experiments that introduce elements of fear to rats at play. The author describes the resulting fearful behavior and quantifies the fluctuation in play that results, and then he investigates how these are modified by increased maternal care or the use of benzodiazepines. In conclusion, he discusses how such research can help shed light on the neurobiology underlying human anxiety disorders, espeically in children

Effects of Neonatal Handling on Play and Anxiety in F344 and Lewis Rats

Play is an important part of normal childhood development and seen in many mammals, including rats. To better understand the interplay between genotype and postnatal experiences, the effects of neonatal handling on play were assessed in Lewis (LEW) and Fischer 344 (F344) rats. Handled litters experienced brief periods of separation during the first two postnatal weeks. F344 rats were less likely to direct nape contacts toward an untreated Sprague–Dawley (SD) partner and less likely to rotate to a supine position in response to a nape contact. When compared to rats from control litters, handled LEW, and F344 rats were more likely to respond to nape contacts with complete rotations, suggesting that handling increased playful responsiveness to a comparable extent in both strains. SD rats paired with handled inbred rats had more nape contacts than those paired with non‐handled rats. While handled LEW rats also tended to direct more nape contacts to the SD partner than non‐handled LEW rats there was no difference between handled and non‐handled F344 rats. These results could not be readily explained by handling‐induced changes in either maternal care or anxiety. These data suggest that the behavioral consequences of neonatal handling may not depend to a great extent on the genetic platform that these manipulations are acting on. These data also suggest that the ability to maintain the ebb and flow between playful solicitation and playful responsiveness may be compromised in F344 rats and may contribute to the lower levels of play in this strain

Effects of Pre-pubertal Social Experiences on the Responsiveness of Juvenile Rats to Predator Odors

The extent to which social variables may modulate the fear associated with a predator cue was assessed in juvenile rats. Cat odor reduced play to a comparable extent in both socially housed and isolate-housed rats, although socially housed rats exhibited more risk assessment during extinction. Rats that had played previously in the context used for assessing fear hid slightly less when exposed to cat odor than those rats that had not played previously in the testing context. However, no other differences were found between these two groups suggesting that prior social experience with the testing context has minimal effects on fear. In a direct test of a \u27social buffering\u27 hypothesis, rats that were tested for contextual fear conditioning in the presence of an unfamiliar partner were less fearful than those rats tested alone. These data are consistent with a social buffering hypothesis and suggest that positive social cues may help animals cope with the threat of predation

Effects of Chlordiazepoxide on Predator Odor-Induced Reductions of Playfulness in Juvenile Rats

The extent to which a non-sedative dose of chlordiazepoxide (CDP) is able to modify the behavioral responses toward a predator odor was assessed in juvenile rats. Play behavior was suppressed and defensive behaviors were enhanced in the presence of a collar previously worn by a cat, when tested 24 hours later in the same context as that where the exposure occurred, and when tested in a context different than that in which the exposure occurred for up to 3 hours after exposure. CDP had no effect on the ability of cat odor to suppress play when rats were tested in the presence of the odor or when tested 24 hours later in the same context where that exposure occurred. When rats were exposed to a worn cat collar in their home cage and tested in a different context CDP attenuated the ability of cat odor to reduce one measure of play (nape contacts) but not another measure (pins). Rats had an opportunity to hide during testing and CDP either decreased hiding or increased risk assessment from within the hide box in all of the testing scenarios. These data suggest that CDP can alter the defensive strategy used by juvenile rats that are confronted with a predatory threat and can also lead to an earlier return to pre-threat levels of playfulness when that threat becomes less immediate

Serotonin, Motivation, and Playfulness in the Juvenile Rat

The effects of the selective 5HT1A agonist 8-OH-DPAT were assessed on the play behavior of juvenile rats. When both rats of the test pair were comparably motivated to play, the only significant effect of 8-OH-DPAT was for play to be reduced at higher doses. When there was a baseline asymmetry in playful solicitation due to a differential motivation to play and only one rat of the pair was treated, low doses of 8-OH-DPAT resulted in a collapse of asymmetry in playful solicitations. It did not matter whether the rat that was treated initially accounted for more nape contacts or fewer nape contacts, the net effect of 8-OH-DPAT in this model was for low doses of 8-OH-DPAT to decrease a pre-established asymmetry in play solicitation. It is concluded that selective stimulation of 5HT1A receptors changes the dynamic of a playful interaction between two participants that are differentially motivated to play. These results are discussed within a broader framework of serotonergic involvement in mammalian playfulness

The Energetic Costs of Rough and Tumble Play in the Juvenile Rat

The metabolic costs of rough-and-tumble play behavior were studied in juvenile rats. Using indirect calorimetry, it was determined that energy expenditure during play is increased by 66-104% over the resting metabolic rate, indicating that play accounts for between 2% and 3% of the total daily energy budget of the rat. In a subsequent experiment, food intake and body weight were monitored for three weeks in rats allowed to play for one hour per day and in rats not allowed to play. While the body weights of the two groups did not differ significantly from each other, those rats allowed to play ate 7% more over the three week period that did those rats not given an opportunity to play. These data are consistent with previous reports describing the energetic costs of mammalian play with play accounting for less than 10% of the daily energy budget in three species tested so far. These data are also consistent with viewing play as a type of exercise and may lead to a better understanding of putative benefits of this behavior

Effects of Amphetamine on Striatal Dopamine Release, Open-Field Activity, and Play in Fischer 344 and Sprague–Dawley Rats

Previous work from our laboratories has shown that juvenile Fischer 344 (F344) rats are less playful than other strains and also appear to be compromised in dopamine (DA) functioning. To determine whether the dysfunctional play in this strain is associated with deficits in the handling and delivery of vesicular DA, the following experiments assessed the extent to which F344 rats are differentially sensitive to the effects of amphetamine. When exposed to amphetamine, striatal slices obtained from F344 rats showed a small increase in unstimulated DA release when compared with slices from Sprague–Dawley rats; they also showed a more rapid high K+-mediated release of DA. These data provide tentative support for the hypothesis that F344 rats have a higher concentration of cytoplasmic DA than Sprague–Dawley rats. When rats were tested for activity in an open field, F344 rats presented a pattern of results that was consistent with either an enhanced response to amphetamine (3 mg/kg) or a more rapid release of DA (10 mg/kg). Although there was some indication that amphetamine had a dose-dependent differential effect on play in the two strains, play in F344 rats was not enhanced to any degree by amphetamine. Although these results are not consistent with our working hypothesis that F344 rats are less playful because of a deficit in vesicular release of DA, they still suggest that this strain may be a useful model for better understanding the role of DA in social behavior during the juvenile period