Neural Correlates of Theory-of-mind Are Associated With Variation in Children's Everyday Social Cognition

Cora E. Mukerji; Sarah Hope Lincoln; David Dodell-Feder; Charles A. Nelson; Christine I. Hooker

Disclosures

Soc Cogn Affect Neurosci. 2019;14(6):579-589. 

In This Article

Abstract and Introduction

Abstract

Theory of mind (ToM), the capacity to reason about others' mental states, is central to healthy social development. Neural mechanisms supporting ToM may contribute to individual differences in children's social cognitive behavior. Employing a false belief functional magnetic resonance imaging paradigm, we identified patterns of neural activity and connectivity elicited by ToM reasoning in school-age children (N = 32, ages 9–13). Next, we tested relations between these neural ToM correlates and children's everyday social cognition. Several key nodes of the neural ToM network showed greater activity when reasoning about false beliefs (ToM condition) vs non-mentalistic false content (control condition), including the bilateral temporoparietal junction (RTPJ and LTPJ), precuneus (PC) and right superior temporal sulcus. In addition, children demonstrated task-modulated changes in connectivity among these regions to support ToM relative to the control condition. ToM-related activity in the PC was negatively associated with variation in multiple aspects of children's social cognitive behavior. Together, these findings elucidate how nodes of the ToM network act and interact to support false belief reasoning in school-age children and suggest that neural ToM mechanisms are linked to variation in everyday social cognition.

Introduction

During middle childhood and early adolescence, children navigate complex social landscapes. Psychosocial challenges, such as school transitions, can exacerbate individual differences in social competence, widening the gap between socially adept children and less-skilled peers (Monahan & Steinberg, 2011). Poor interpersonal functioning is associated with negative outcomes, including lower academic achievement, problem behaviors and psychopathology (Elliott et al., 2001; Spence, 2003). To develop targeted interventions, it is critical to understand mechanisms that contribute to variation in children's social functioning.

Social competence depends, in part, upon theory of mind (ToM). ToM allows us to represent others' mental states, predict what they might do next and generate an appropriate response. False belief (FB) understanding is an early emerging ToM capacity widely assessed in the developmental literature (Wellman et al., 2001). To reason about FBs, a child must understand that the content of a person's beliefs can contradict reality, providing evidence of representational ToM (Wimmer & Perner, 1983). Between ages 3 and 5, children demonstrate above-chance performance on explicit FB tests. FB performance in early childhood predicts real-world social behavior, including mind-reading (De Rosnay et al., 2014), popularity (Slaughter et al., 2015) and social competence (Devine et al., 2016). These findings suggest that ToM mechanisms contribute to variation in social development.

Cognitive neuroscience research in adults has revealed a distributed set of neural regions supporting FB reasoning (Gallagher et al., 2000; Saxe & Kanwisher, 2003): the bilateral temporoparietal junction (RTPJ and LTPJ), precuneus (PC), medial prefrontal cortex (MPFC) and right superior temporal sulcus (RSTS). Prior functional magnetic resonance imaging (fMRI) studies in smaller samples indicate that children, ranging in age from 5 to 13, may recruit the same regions for ToM reasoning, suggesting the broader architecture of this ToM 'network' emerges early in childhood (Ohnishi et al., 2004; Kobayashi et al., 2007; Saxe et al., 2009; Gweon et al., 2012). However, neural ToM mechanisms may not yet be functionally mature. Preliminary studies suggest that children demonstrate increasing specialization of the TPJ for mental state content with age (Saxe et al., 2009; Gweon et al., 2012). In addition, youths demonstrate decreasing MPFC activation with age across a variety of mental state reasoning (i.e. mentalizing) tasks, suggesting continued maturation from preadolescence into adulthood (Blakemore, 2012).

Although this set of regions is conceptualized as a network, few studies have explored how these nodes interact to support ToM. Previous studies of ToM-related neural connectivity in children have employed different tasks and analyses at different ages, yielding distinct results. Recent work employing inter-region correlation analysis has indicated positive associations between ToM regions during passive viewing of an animated film in children (ages 3–12), suggesting emerging integration within the ToM network (Richardson et al., 2018). However, correlational approaches are limited in their ability to identify patterns of functional connectivity specific to mentalizing vs other cognitive processes. Psychophysiological interaction (PPI) analysis can help evaluate such questions by examining effective connectivity, i.e. the influence of activity in one neural region upon another, elicited by a certain task (Friston, 2011). For example, PPI analyses indicate greater frontotemporal connectivity when mentalizing about social vs non-social emotions in adolescents compared to adults, suggesting developmental changes in patterns of connectivity that support social–emotional reasoning (Burnett & Blakemore, 2009). Further work is needed to evaluate the functional integration of ToM regions when reasoning about other mental states (e.g. beliefs) during childhood.

Although ToM is considered central to social development, few neuroimaging studies have directly evaluated this hypothesis. Developmental fMRI studies have yielded preliminary evidence that functional specialization of the RTPJ (Gweon et al., 2012) is associated with performance on lab-based ToM tasks. In addition, parent-reported ToM abilities have been linked to connectivity of the RTPJ with other ToM regions at rest (Xiao et al., 2019). While studies in adults have implicated the LTPJ in facilitating general perspective-taking (Schurz et al., 2013) and the PC in mental imagery (Cavanna & Trimble, 2006), relatively little is known about the role of these ToM regions in supporting social cognition in childhood. Moreover, relations between task-modulated activity or connectivity in the ToM network and children's social cognition in everyday contexts remain unclear.

Empathy, the capacity to represent and share the emotional experiences of others, is a related social cognitive process that is fundamental to social interaction (Singer & Tusche, 2014). Although representation of another's affective experience is central to empathy, ToM and empathy rely––in part––upon overlapping neural mechanisms. Empathy engages core nodes of the ToM network (including the TPJ and PC/posterior cingulate cortex), in addition to other neural circuitry supporting affective sharing (Völlm et al., 2006; Zaki et al., 2009; Bzdok et al., 2012). Further research is needed to explore whether neural ToM mechanisms contribute to variability in children's empathy in everyday settings, as well as other facets of social cognition.

In the current study, participants (ages 8–13) completed an FB fMRI task adapted for children. First, we aimed to test neural activity elicited by reasoning about FBs vs non-mentalistic false content (False Belief>False Photo; FB>FP), allowing us to identify regions specifically engaged by ToM processing during this developmental period. Second, we aimed to evaluate functional integration of key ToM regions. Generalized PPI analyses (gPPI) were used to examine effective connectivity between regions of interest (ROIs) in the ToM network during FB>FP, elucidating ToM-modulated changes in connectivity. Last, we aimed to explore associations between these neural ToM measures and multiple facets of everyday social cognition, including empathy. Therefore, we tested whether neural activity and effective connectivity in the ToM network explained variance in children's self- and parent-reported social cognitive behavior. We predicted that when reasoning about FBs (FB>FP), school-age children would demonstrate (i) enhanced activation in key ToM regions and (ii) greater effective connectivity between these regions. Moreover, we expected (iii) the magnitude of task-modulated activity and connectivity would be associated with variation in children's social cognition in everyday settings.

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