Towards a neuroscientific understanding of play: A neuropsychological coding framework for analysing infant-adult play patterns

During early life, play is a ubiquitous activity, and an individual’s propensity for play is positively related to cognitive development and emotional well-being. Play behaviour is diverse and multi-faceted. A challenge for current research is to converge on a common definition and measurement system for play ‒ whether examined at a behavioural, cognitive or neurological level. Combining these different approaches in a multi-level analysis could yield significant advances in understanding the neurocognitive mechanisms of play, and provide the basis for developing biologically-grounded play models. However, there is currently no integrated framework for conducting a multi-level analysis of play that spans brain, cognition and behaviour. The proposed neuropsychological coding framework uses grounded and observable behaviours along three neuropsychological dimensions (sensorimotor, cognitive and socio-emotional), to compute inferences about playful behaviour and related social interactional states. Here, we illustrate the sensitivity and utility of the proposed coding framework using two contrasting dyadic corpora (N=5) of mother-infant object-oriented interactions during experimental conditions that were either conducive (Condition 1) or non-conducive (Condition 2) to the emergence of playful behaviour. We find that the framework accurately identifies the modal form of social interaction as being either playful (Condition 1) or non-playful (Condition 2), and further provides useful insights about differences in the quality of social interaction and temporal synchronicity within the dyad. In conclusion, here, we present a novel neuropsychological framework for analysing the continuous time-evolution of adult-infant play patterns, underpinned by biologically informed state coding along sensorimotor, cognitive and socio-emotional dimensions. We expect that the proposed framework will have wide utility amongst researchers wishing to employ an integrated, multi-level approach to the study of play, and lead towards a greater understanding of the neuroscientific basis of play and may yield insights into a new biologically-grounded taxonomy of play interactions.

coded (e.g. touching a toy, looking at a toy, smiling, etc), and the presence or absence of play 1 (and other related social states) is inferred from temporally co-occurring patterns of 2 behaviour. 3 The joint social state of adults and infants can also be assessed using this scheme. For 4 example, during didactic teaching, only the cognitive dimension may be concurrently 5 engaged in both partners, whilst their sensorimotor and socio-emotional states may be 6 discordant (e.g. Mother's state is [1 1 0] whilst the infant's state is [0 1 1]). Importantly, this 7 framework permits an empirical discrimination between similar/related social interactional 8 states such as teaching versus play. Although the play-congruent state [1 1 1] is of greatest 9 interest here, a total of 8 different social states for infants and adults (and 64 joint adult-infant 1 0 states) may be discriminated under the proposed framework, which may yield insights into a 1 1 new biologically-grounded taxonomy of play interactions. Here, we illustrate the application of our proposed neuropsychological play coding 1 4 framework using examples from two contrasting dyadic corpora of mother-infant object-1 5 oriented interactions during experimental conditions that were either conducive (Condition 1) 1 6 or non-conducive (Condition 2) to eliciting playful behaviour. In Condition 1, playful 1 7 behaviour was encouraged by asking mothers to use the objects in spontaneous, fun and 1 8 natural interactions with their child. In Condition 2, playful behaviour was discouraged by 1 9 asking mothers to focus on teaching infants about the social value (desirable or non-2 0 desirable) of the objects. These corpora comprise both behavioural and 2 1 electroencephalography (EEG) measurements that were collected concurrently from mothers 12 Running Head: A Neuropsychological Coding Framework for Play 12 and their infants. However, for this study, we focus solely on behavioural analyses only. We 1 have two specific sets of predictions regarding the differences between conditions that should 2 emerge following application of the coding framework: 3 1) In Condition 1 (conducive), infants' modal state will be [1 1 1] (i.e. play-congruent along 4 all three dimensions), but in Condition 2 (non-conducive), [1 1 1] will not be the modal 5 state; 6 2) In Condition 1 relative to Condition 2, infants will show: The first prediction pertains to the sensitivity of the coding framework in detecting 1 1 play-related behaviour. Simply put, if mothers were instructed to play with their infants, then 1 2 (although coders do not make direct judgements about whether participants were playing or 1 3 not) we expect the coding framework to reveal that a play-congruent state was indeed the 1 4 most frequent social state that infants displayed. The second set of predictions pertains to the 1 5 utility of the framework in identifying differences in the quality of social interaction and 1 6 temporal synchronicity with the dyad. Condition 1 (not play-conducive). In this condition, mothers were asked to teach their 2 infants about the social value of pairs of ambiguous novel objects. For each pair of objects, 3 mothers were instructed to describe one object with positive affect ("This is great, we really 4 like this one!") and the other object with negative affect ("This is bad, we don't like this 5 one"), as shown in Figure 1. Mothers were asked to limit their verbal descriptions to four 6 simple formulaic sentences per object (which they repeated for each object), and to model 7 positive or negative emotions in a prescribed manner (e.g. smiling versus frowning). The 8 order of object presentation (positive or negative) was counterbalanced across trials. After 9 observing their mothers' teaching about both objects, infants were then allowed to interact 1 0 briefly with the objects themselves before the objects were retrieved. During the session, an 1 1 experimenter was present to ensure that participants were interacting as instructed. She   Condition 2 (play-conducive). In this condition, mothers were asked to play with their 2 1 infant using a set of attractive toys (see Figure 2). Mothers were instructed to use the toy 15 Running Head: A Neuropsychological Coding Framework for Play 15 objects in a spontaneous, fun and natural way, to actively engage the infant's attention, but to 1 play quietly whilst avoiding large physical motions (in order to minimise EEG motion 2 artifacts). During the session, an experimenter was present to ensure that participants were  To record the actions of the participants, two Logitech High Definition Professional 1 5 Web-cameras (30 frames per second) were used, directed at the adult and infant respectively.

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Afterwards, each video recording was manually coded for the timing of the behaviours of 1 7 interest, using the coding scheme outlined in Section 2.5.

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EEG data was also concurrently collected from mothers and infants during social 1 9 interactions, but this data is not reported here as the primary focus of the current study is to 2 0 develop a framework for assessing play behaviour. Attention is focused on the object or partner with object-specific exploration of object 3 Attention is focused on the object or partner with pretence/acting behaviour related to object 4 Attention is focused on the object or partner with rule-based behaviour related to object 5 Attention is not on the object or partner 0 - The term 'play-congruent' is used to refer to behaviours and states in each dimension 2 during which play might be occurring, and where the individual might be in a playful mental 3 frame. Initially, we sought to base our model around the broadest criteria for a play-congruent 4 state, and then ensure that states based on narrower criteria could also be discriminated. In 5 each dimension, the presence of play-congruent behaviour is allocated a code of 1 and the 6 absence of play-congruent behaviour is allocated a code of 0 (see 'Code' column in Table 1).

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When play-congruent behaviour is concurrently observed across all three dimensions (i.e. [1 8 1 1]), the resulting state is termed a 'play-congruent state'. This model can be used to explore 9 how individuals move into and out of these broadly-defined play-congruent states (and in 1 0 future, to explore related neural activity), as illustrated in Section 2.6.

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Note that due to the flexibility of the model, it is also possible to analyse how deemed as congruent with a play-state in the sensorimotor dimension. infant swinging a toy around while not looking at anything in particular, or with eyes closed), 19 Running Head: A Neuropsychological Coding Framework for Play we decided that, as we were interested in play's effects at the neural level, even our broadest 1 criteria for a play-congruent state should include some level of cognitive engagement. In 2 other words, our model is intended to explore 'minds-on' play, rather than 'minds-off' play 3 that is purely physical or sensory in nature. Therefore, visual attention on either the object or 4 the play partner was deemed as congruent with a play-state in the cognitive dimension.

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In the cognitive dimension five sub-codes were also developed to delineate whether 6 the individual is also engaged in exploratory behaviour (object-general or object-specific), 7 pretence or acting, or rule-based behaviour. The distinction between object-general and 8 object-specific exploration is intended to capture two different levels of cognitive 9 engagement which are expected to relate to observable differences in neural activity. Object-1 0 general exploration is any kind of activity with the object that does not involve appreciation 1 1 of the object's particular properties, i.e. the action could be done with almost any object. The unlikely to lead to specific conceptual information about an object's functions and uses.

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Object-specific exploration, by contrast, involves an appreciation of that object's unique 1 7 properties -for example, spinning the blades of a toy helicopter, pushing on the surface of a 1 8 balloon, or pulling on parts of the object to see if they can be removed. It is this kind of 1 9 exploration that seems most likely to lead to more advanced conceptual learning about an 2 0 object's functions and uses. Figure 3 shows an example of the resulting codes for each 2 1 separate dimension over time during a social interaction episode for an infant: proportion of time during which the infant has active "hands-on" possession of the toy (e.g.    interaction are occurring (as well as their timing and frequency of occurrence). Accordingly, 1 6 we next assessed infants' social states (calculated for each timepoint) in each condition.

Frequency distribution of social states during play and teaching
1 8 The frequency distribution of different social states observed in infants and mothers 1 9 during Conditions 1 and 2 are shown in Figure 7. Given that there were only 5 data points,   conditions. There was a significant decrease in the frequency of the play-incongruent social 27 Running Head: A Neuropsychological Coding Framework for Play 27 state of [0 1 1] (negative affect, contact, attention) in Condition 2 as compared to Condition 1 1 (t(4) = -9.85, BH-FDR p<.01). However, although there was a trend toward an increase in 2 play-congruent behaviour ([1 1 1]) in mothers for Condition 2, this increase was not 3 significant (t(4) = 1.28, BH-FDR p=.43). Therefore, although mothers displayed less play-4 incongruent behaviour during Condition 2 than Condition 1, we did not observe significantly 5 more play-congruent behaviour. interactions that were non-conducive to playful behaviour, infants were predominantly 1 2 passive ("hands-off") but attentive. During social interactions that supported playful 1 3 behaviour, infants were predominantly active ("hands-on"), positive and attentive.

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Adults. By contrast, mothers displayed almost no difference in their modal states

Mother-infant joint states (behavioural state synchrony)
2 0 Finally, we assessed the joint probability distribution of infants' and mothers' social 2 1 28 Running Head: A Neuropsychological Coding Framework for Play 28 states during Conditions 1 and 2, as shown in Figure 8. Of note, perhaps the most relevant 1 difference is that during Condition 1, mothers and infants were in a joint play-congruent 2 social state (i.e. [1 1 1] -[1 1 1], or synchronous play) only 5.7% of the time on average. By 3 contrast, during Condition 2, mothers and infants showed synchronous play 24.9% of the 4 time -a nearly five-fold increase. Therefore, during conducive social contexts (Condition 2), 5 the play-congruent state occurred more frequently in regard to infants' own behaviour, and 6 this joint social state also occurred concurrently (i.e. synchronously) with their mothers more Play behaviour is diverse and multi-faceted, and a major challenge for current 2 research is to converge on a common definition and measurement system for play that 3 integrates behavioural, cognitive and neurological levels of analyses. Here we present and 4 test a new methodological framework that captures different social interactional states (play-5 congruent or play-incongruent) and permits an empirical discrimination between similar and 6 related social interactional states (such as joint activities in situations both conducive and 7 non-conducive to the emergence of playful behaviour).

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A-priori, we made two sets of predictions about the differences in infants' behaviour 9 between these conditions and our coding results supported both predictions. First, we 1 0 observed that during conducive social interactions, infants' modal state was indeed play- playful or non-playful, even though coders did not explicitly code for play itself. Further, our 1 6 data also highlight the fact that, although mothers were instructed to play with their infants data that is collected during such play sessions. If infants' neural data during play is assumed 2 2 to be homogenous and analysed as such (e.g. by computing averages of neural indices across 1 all time-points), such an analysis would be erroneous as it would include many periods when 2 play is not actually occurring. The proposed coding framework therefore lends itself well to 3 time-sensitive neural analyses, because it permits the automatic extraction of discrete time 4 periods when a playful social state is observed (i.e. [1 1 1]), as well as separate analyses of 5 the periods leading up to, and away from these moments.

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As predicted, our coding results also showed that, when infants were engaged in 7 social interactions that were conducive for playful behaviour (Condition 2), they showed 8 decreased negative affect, increased sensorimotor involvement with objects, but equivalent 9 attentional engagement. Similarly, mothers also showed significantly decreased negative social context for early learning as compared to direct didactic instruction from parents.

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Finally, we observed that during play, parent-child dyads showed greater temporal  (Kaye & Fogel, 1980), affect (Cohn & Tronick, 1988Feldman et al, 2011) and even 1 autonomic arousal (Feldman et al, 2011;Waters et al, 2014). Our coding scheme not only 2 allows the identification of specific time periods when play is synchronously occurring 3 between mother and child (e.g. for neural analyses), but also allows comparison to periods 4 when the dyad is socially asynchronous, or 'out of tune' with each other. Such parent-child 5 asynchrony is known to occur more frequently and to be of particular clinical relevance in 6 affective disorders such as maternal depression (Goldsmith & Rogoff, 1997;Jameson et al, 7 1997).

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One major limitation to the current study is its small sample size. However, our 9 intention has been to illustrate the sensitivity of the proposed framework in discriminating 1 0 between different play-related states, using a coding scheme grounded in simple, observable 1 1 behaviour and with a temporal resolution suited to neuroscientific research. Five dyads 1 2 provided sufficient data to assess the efficacy of the framework as a means of capturing 1 3 variations in individual and joint behaviour as continuously evolving states, rather than as 1 4 discrete actions or a subjective global assessment. Nevertheless, research applying our 1 5 framework to larger samples is needed to ensure that the contextual differences we identified 1 6 between play and teaching scenarios are generalisable.

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A second limitation is our focus on one specific type of play which revolves around a 1 8 physical object. However, the focus on a physical object does not limit our model entirely to 1 9 the earlier and more basic types of play, because a physical object can be used in play with 2 0 more symbolic content. For example, object substitution -using an object as if it is 2 1 something else -is often coded in established play coding schemes as an indicator of pretend 32 Running Head: A Neuropsychological Coding Framework for Play 32 play. Many games with rules involve physical objects, so participants could engage in such a 1 game, either spontaneously or because they are asked to do so. We decided to capture these 2 more complex types of behaviour in our model, with the acknowledgement that in infancy, 3 these types of behaviour will be very rare, and most likely observed on the part of the parent. 4 Also, with appropriate development (e.g. the elaboration of sub-code options) our framework 5 could be applied to more abstract forms of play that do not revolve around physical objects.

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A final limitation is that, as play behaviour changes significantly across the life-span 7 (Power, 1999), we chose to focus primarily on infants. Therefore, adult play behaviour may 8 not have been optimally-captured by the framework. Nonetheless, our coding revealed an 9 interesting result: mothers (unlike their infants) did not show a clear shift toward greater 1 0 playfulness for Condition 2 as compared to Condition 1, although their negative affect 1 1 decreased overall. One possible reason for this may be that mothers approached the teaching 1 2 exercise in Condition 1 as pretend play. Since the objects used in Condition 1 had no intrinsic 1 3 social value, mothers had to act out a 'good' or 'bad' response to the objects, by pretending 1 4 that the objects had a particular social significance. However, it is clear from our data that 1 5 infants (aged on average 10.7 months) responded less playfully to their mother's social 1 6 pretend play, consistent with the late emergence of pretend play capabilities during the 1 7 second year of life (Fein, 1981).

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Although the neural EEG data that was collected during the parent-child social 1 9 interactions was not analysed here, the proposed framework represents an important first step 2 0 towards conducting meaningful analyses of these neural data. Specifically, since the proposed 2 1 framework fractionates play behavior along neuropsychological dimensions, this provides the 33 Running Head: A Neuropsychological Coding Framework for Play 33 capability for (1) internal prediction and validation (e.g. during periods of sensorimotor 1 activity only, neural activity should predominantly arise from the sensorimotor cortices) and 2 (2) the identification of common neural substrates that underlie play-related social 3 interactional states. An analysis of these underlying neural substrates may, in future, lead to a 4 definition of play behaviour that is more closely grounded in neuroscience. The further 5 subcategories of different types of cognitive interaction also included in the scheme (see 6   Table 1) will also allow us to look, in more detail, at other types of play. For example, it may 7 be of interest to assess whether the use of pretend play by parents (for example, when the 8 mother pretends that a ball is an animal) is related to the early development of pretense 9 capabilities in infants. In adults, the observation of substitute object pretense leads to activity 1 0 in the superior parietal lobule (Smith et al, 2013). If the observation of object substitution in 1 1 infancy was also found to lead to similar patterns of neural activation, this may provide 1 2 neurological evidence for the facilitation of an emerging awareness of pretence in infants in 1 3 response to parental pretend play.

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In conclusion, we have presented a novel neuropsychological framework for dimensions. We expect that the proposed framework will have wide utility amongst 1 8 researchers wishing to employ an integrated, multi-level approach to the study of play, and 1 9 lead towards a greater understanding of the neuropsychological basis of play.