Frontiers in Human Neuroscience, 01 October 2020 https://doi.org/10.3389/fnhum.2020.560176
- 1Department of Psychology, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, United Kingdom
- 2School of Psychology, Cardiff University, Cardiff, United Kingdom
- 3School of Psychology, Cardiff University Centre for Human Developmental Science (CUCHDS), Cardiff, United Kingdom
- 4School of Psychology, Cardiff University Brain Research Imaging Centre (CUBRIC), Cardiff, United Kingdom
It has long been hypothesized that pretend play is beneficial to social and cognitive development. However, there is little evidence regarding the neural regions that are active while children engage in pretend play. We examined the activation of prefrontal and posterior superior temporal sulcus (pSTS) regions using near-infrared spectroscopy while 42 4- to 8-year-old children freely played with dolls or tablet games with a social partner or by themselves. Social play activated right prefrontal regions more than solo play. Children engaged the pSTS during solo doll play but not during solo tablet play, suggesting they were rehearsing social cognitive skills more with dolls. These findings suggest social play utilizes multiple neural regions and highlight how doll play can achieve similar patterns of activation, even when children play by themselves. Doll play may provide a unique opportunity for children to practice social interactions important for developing social-emotional skills, such as empathy.
Although children’s play is studied extensively, a definition as to what play is has not yet reached consensus (for a review, see Lillard, 2014). When children are asked, they describe playing as simply something they find fun (Downey et al., 2007). It is however generally agreed that play appears in many different forms including pretend or symbolic play, games with rules, language play, rough-and-tumble play, and construction play (Burghardt, 2010).
One of the more recognized and researched forms of play is “pretend play” (or symbolic play or fantasy play), where children playfully distort reality to behave in a nonliteral, “as if” mode (Fein, 1981). A common element of children’s pretend play is the presence of toys and dolls which act to encourage children’s pretense (Singer and Singer, 1990). Pretend play was originally argued to emerge when children reach the age of two and thereafter declines between the ages of four and seven (Piaget, 1962). However, it is increasingly recognized that play, and pretend-play in particular, continues beyond this age (e.g., Singer and Singer, 2005; Lillard, 2014).
Pretend play is argued to provide benefits in the development of social processing (Lillard, 2017) and executive function (see Carlson and White, 2013; Sachet and Mottweiler, 2013). Regular play with others provides advantages in aspects of social understanding, in terms of references to the thoughts and feelings of others (Youngblade and Dunn, 1995; Howe et al., 2014; Tessier et al., 2016), perspective taking (Dunn and Cutting, 1999; Harris, 2000), and empathy (Brown et al., 2017). However, the correlational nature of these studies limit conclusions regarding causation (see Lillard et al., 2013). In terms of children’s executive function, evidence from both correlational and intervention studies have found “pretend-play” to be associated with improvements in executive function skills (Albertson and Shore, 2009; Kelly and Hammond, 2011; Thibodeau et al., 2016), as children must inhibit reality to maintain the imagined components of play (Carlson et al., 2014), and use their working memory to retain and recall information regarding their play (Pierucci et al., 2014).
Although, play is considered a largely social activity (Lillard, 2017), pretend play can occur in both social contexts with a play partner and in the solitary form (Garvey, 1974), and solitary play is considered to be a preference for some children (Coplan et al., 2014; Ooi et al., 2018). Indeed, in one survey of children between the ages of 4 and 12, over a third of children reported playing with dolls and toys as one of their favorite activities, but only when playing alone, and this was mostly reported by the younger children (Downey et al., 2007). However, Piaget (1962) contended that all pretend play activities are social to an extent, as even solitary pretend play is a performance to an imaginary other.
Play in the Brain
Limited research has investigated brain activation during children’s play. Due to the practical challenges of measuring brain activity during natural play, most research into the neural correlates of social interactions has used highly controlled tasks that have examined electrical activity (electroencephalography, EEG) or blood flow (functional near infrared spectroscopy, fNIRS) during episodes of brief social interaction or observation of social stimuli (e.g., mutual gaze or infant-directed speech) vs. lack of social interaction or observation of social stimuli (e.g., lack of eye contact or non-social stimuli). For example, Lloyd-Fox et al. (2009, 2015) have found activation in fNIRS optodes consistent with posterior superior temporal sulcus (pSTS) activation during processing of social and communicative stimuli, relative to non-social and non-communicative stimuli in infants and toddlers (Hakuno et al., 2018). These findings are consistent with pSTS being recruited during social interactions and social processing (e.g., the theory of mind) in functional magnetic resonance imaging (fMRI) studies in adults (Redcay et al., 2010; Lahnakoski et al., 2012; Deen et al., 2015). Whether naturalistic play activates these same brain regions is, as yet, unknown. Given that the pSTS is active during minimal social interactions in lab settings (e.g., shared attention on a toy), one would expect that active and natural play with another person would activate this region, especially when engaging in pretend play that enables social perspective-taking and representation of others’ emotions and thoughts.
The neural correlates of executive function are relatively well established across paradigms and ages. fMRI, EEG, and fNIRS research all indicate that the prefrontal cortex (PFC) is activated during executive functioning tasks that include inhibition and working memory (Burgess and Stuss, 2017). In preschool-aged children, for whom executive functioning skills are still emerging, individual differences in executive functioning correlate with differences in brain activation of this region. For example, in an fNIRS study with 3- and 5-year-olds, Moriguchi and Hiraki (2009) found that prefrontal areas were only activated during executive function tasks for those children who successfully performed the task and not those who made errors. Similar findings of individual differences in executive function skills relating to cortical activation of the PFC region have been found in adults using fNIRS (Yasumura et al., 2014). As far as we are aware, direct measurement of prefrontal activity during natural play that involves executive function skills like planning and inhibition has not been carried out.
The orbitofrontal cortex (OFC) is associated with reward processing and positive affect (Berridge and Kringelbach, 2008). For example, Minagawa-Kawai et al. (2009) found greater OFC activation (using fNIRS) when infants viewed their own mothers’ smiles than when they viewed an unfamiliar mother’s smile. In mothers, OFC activation was specific to viewing their infants, relative to unfamiliar infants, and was related to behavioral ratings of pleasant mood. Similar effects of rewarding and motivating stimuli on OFC have been found across multiple methodologies and ages (e.g., May et al., 2004; Kida and Shinohara, 2013). If children find certain kinds of play particularly rewarding and motivating, OFC activation should evidence this.
In the current research, we investigate the unique neural correlates of pretend play (in the form of doll play) relative to other play (tablet games) in a naturalistic setting. We collected fNIRS data from 4- to 8-year-old children while they engaged in varying forms of play either alone or with a social partner (i.e., an experimenter). Children in this age range were old enough to follow directions, play on their own, and maintain attention for the duration of the task but were young enough to engage in natural play in these settings. As a contrast to doll play, tablet games were chosen that allowed creative and open play (i.e., no set rules or objectives) and were suitable for this age range but did not involve doll play. In the chosen tablet games (described in more detail in the “Materials and Methods” section), children cut and styled hair or built towns. We included both solo and joint play to examine whether brain activity was different when children engaged in these forms of play by themselves or with a social partner. Our regions of interest (ROIs) covered elements of functional networks related to empathy and perspective taking (pSTS; Hakuno et al., 2018), executive function (PFC; Moriguchi and Hiraki, 2009), and reward-seeking (OFC; Minagawa-Kawai et al., 2009). Our key questions concerned which brain areas would be selectively engaged during doll play, relative to tablet play, and whether this was consistent across the solo and joint play.