Age-related differences in function and structure of rSMG and reduced functional connectivity with DLPFC explains heightened emotional egocentricity bias in childhood

doi:10.1093/scan/nsu057 SCAN (2015) 10, 302^310 Age-related differences in function and structure of rSMG and reduced functional connectivity with DLPFC explains heightened emotional egocentricity bias in childhood Nikolaus Steinbeis, Boris C. Bernhardt, and Tania Singer Department of Social Neuroscience, Max-Planck Institute for Human Cognitive and Brain Sciences, 04109 Leipzig, Germany Keywords: functional and structural brain development; socio-affective development; emotional egocentricity bias; self–other distinction; supramarginal gyrus; dorsolateral prefrontal cortex INTRODUCTION Humans tend to rely on their own experiences and mental states to infer those of other people (Gallese and Goldman, 1998; Singer et al., 2004; Keysers and Gazzola, 2007). This works efficiently when mental states between oneself and others align, but such a mechanism will betray a bias to judging others egocentrically when this is not the case, for example, judging others as happier when they are evidently upset merely because oneself is happy. Children are particularly prone to various kinds of blatant egocentricity (Piaget and Gabain, 1932; Kohlberg, 1984). Although the majority of the evidence for such egocentricity comes from studying the development of cognitive perspective-taking and theory of mind (Elkind, 1967; Flavell, 1999; Royzman et al., 2003), very little is known in contrast about how emotional egocentricity manifests itself in development and what the underlying neural and associated cognitive processes are that give rise to such emotional egocentricity in childhood. Emotional egocentricity lies at the heart of much of human interpersonal (Thompson and Loewenstein, 1992) and group conflict (Chambers et al., 2006). Peer conflicts are rife in childhood; lacking the ability to resolve them can lead to maladjustment and social rejection (Newcomb et al., 1993), causing problems in life-span development and health (Murphy et al., 2013). Unraveling the mechanisms that give rise to emotional egocentricity in development can, thus, help to identify the causes of this socially detrimental behavior early in life, offering the potential for targeted intervention. To address our first major aim, we wanted to compare the emotional egocentricity bias (EEB) between children and adult. To this Received 20 October 2013; Revised 25 February 2014; Accepted 16 April 2014 Advance Access publication 24 April 2014 This research was funded by the Swiss National Science Foundation (‘‘Neuronal and developmental basis of empathy and emotion control: fMRI studies of adults and children aged 6 to 12 years’’; to T.S.), and the University Research Priority Programs (URPP) of the University of Zurich. Correspondence should be addressed to Nikolaus Steinbeis, Department of Social Neuroscience, Max-Planck Institute for Human Cognitive and Brain Sciences, Stephanstrasse 1a, 04105 Leipzig, Germany. E-mail: . end, we developed a novel paradigm, a performance-based monetary reward and punishment task (the REAP task). Based on previous work on emotional egocentricity in adults (Silani et al., 2013), we refer to EEB when one’s empathic judgments of another persons’ feeling state is biased toward one’s own simultaneously experienced, albeit emotionally incongruent, state. In other words, EEB expresses the inability to disregard one’s own feeling states to accurately judge the state of another, who is feeling something different to oneself. Previous studies have shown that attributing desires to others incongruent with one’s own is something already young children around 18 months successfully do (Repacholi and Gopnik, 1997). However, behavioral evidence suggests that the ability to attribute beliefs and desires to others incongruent to one’s own is protracted and continues into adulthood; in turn, difficulties in such cognitive perspective taking are generally found to be much larger in children (Keysar et al., 2003; Apperly et al., 2011). In spite of this wealth of behavioral studies on egocentricity in the cognitive domain, the developmental trajectory of emotional egocentricity remains unknown. Thus, in addition to investigating the developmental course of EEB from childhood into adulthood using a novel paradigm, we also sought to identify cognitive mechanisms accounting for potential age-differences in EEB. These include attentional reorienting, as well as response inhibition, fluid intelligence, and cognitive perspective-taking (see Supplementary Materials). A second goal of the study was to understand the neuronal mechanisms underlying age-related differences in overcoming such EEB from childhood to adulthood. Adults have been shown to be prone to egocentric judgments both in the cognitive domain (Royzman et al., 2003; Pronin, 2008) as well as when attributing visceral (Van Boven and Loewenstein, 2003; O’Brien and Ellsworth, 2012) and affective states (Silani et al., 2013). A recent study from our group combining transcranial magnetic stimulation (TMS) and functional magnetic resonance imaging (fMRI) was able to demonstrate that, in adults, right supramarginal gyrus (rSMG) is critically involved in overcoming emotional egocentricity when making judgments on the emotional states of ß The Author (2014). Published by Oxford University Press. For Permissions, please email: Humans often judge others egocentrically, assuming that they feel or think similarly to themselves. Emotional egocentricity bias (EEB) occurs in situations when others feel differently to oneself. Using a novel paradigm, we investigated the neurocognitive mechanisms underlying the developmental capacity to overcome such EEB in children compared with adults. We showed that children display a stronger EEB than adults and that this correlates with reduced activation in right supramarginal gyrus (rSMG) as well as reduced coupling between rSMG and left dorsolateral prefrontal cortex (lDLPFC) in children compared with adults. Crucially, functional recruitment of rSMG was associated with age-related differences in cortical thickness of this region. Although in adults the mere presence of emotional conflict occurs between self and other recruited rSMG, rSMG-lDLPFC coupling was only observed when implementing empathic judgements. Finally, resting state analyses comparing connectivity patterns of rSMG with that of right temporoparietal junction suggested a unique role of rSMG for self-other distinction in the emotional domain for adults as well as for children. Thus, childrens difficulties in overcoming EEB may be due to late maturation of regions distinguishing between conflicting socio-affective information and relaying this information to regions necessary for implementing accurate judgments. rSMG maturation and EEB MATERIALS AND METHODS Participants Study 1 (Behavioral) Participants were 168 children (70 boys; mean  s.d. age ¼ 10.14  1.79 years; age range ¼ 7–13 years). The majority (163) of them were Swiss, two were German, one wa (...truncated)