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

Abstract

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, children's 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.

Keywords: dorsolateral prefrontal cortex; emotional egocentricity bias; functional and structural brain development; self–other distinction; socio-affective development; supramarginal gyrus.

Fig. 1

Experimental design and behavioral results. (A) Operationalization of the EEB. (B) In a speeded reaction time task, participants first reacted as fast as they could, then they saw whether both they and the other had won or lost and finally they indicated how they felt. (C) In the fMRI study, participants underwent blocks in which they had to either provide a judgment or not. (D) In Study 1, children showed a significant effect of congruency between their own affective state and that of the other person, whereby they rated the other as feeling more negative when they themselves had lost and more positive when they themselves had won, which (E) resulted in a significant EEB. (F) The EEB in the positive and negative domain were significantly correlated. (G) In Study 2, children showed a significant effect of congruency, whereas adults did not, which (H) led to a significant EEB only in children and not in adults. (I) The EEB during wins and losses was significantly correlated for both children and adults. (J) In Study 1, there was also an age-related decrease in the EEB in the sample of children, and a trend in the sample of children in Study 2.

Fig. 2

fMRI results: (A) When comparing congruent with incongruent trials, adults showed strong activitation of rTPJ and rSMG. (p_fwe < 0.05), whereas (B) children showed activity in right inferior frotal gyrus (P < 0.05 uncorrected). (C and D) The direct comparison between adults and children showed that recruitment of rTPJ and rSMG was stronger in adults than in children (p_svc < 0.005). (E) The group difference between adults and children in rSMG (thresholded at p_svc < 0.005) overlapped with regions previously identified to be crucial for overcoming emotional egocentricity in adults (Silani et al., 2013).

Fig. 3

PPI: (A) When seeding from rSMG, (B) adults with smaller EEB show an increased functional coupling of rSMG and lDLPFC (p_svc < 0.005). (C) In children, on the other hand, those with smaller EEB showed increased functional coupling of rSMG and medial PFC (p_fwe < 0.05). (D) When comparing the association between individual differences in EEB and functional coupling of rSMG, adults showed significantly stronger connectivity with lDLPFC than children (p_svc < 0.005).

Fig. 4

Comparing judgment and no-judgment trials. (A) When children had to provide a judgment, medial PFC was significantly activated (p_fwe < 0.05). (B) For children, medial PFC was activated during runs when a judgment had to be made, compared with when it did not have to be made (p_fwe < 0.05). For adults, rSMG activity was recruited both when (C) a judgment had to be made (p_fwe < 0.05) and (D) also when no judgment had to be made (p_fwe < 0.05). (E) When comparing the functional connectivity with rSMG during runs when a judgment had to be made compared with when it did not, there was greater functional coupling with lDLPFC for adults (p_svc < 0.005).

Fig. 5

Functional connectivity differences between rSMG and rTPJ in children and adults (p_fwe < 0.05). (A) In adults, rSMG showed more marked connectivity relative to rTPJ to bilateral insula and rSMG; conversely, rTPJ was more strongly connected than rSMG to large portions of medial PFC, precuneus, TPJ, the temporal poles and superior frontal gyrus. (B) For children, these patterns were virtually identical, with the exception of increased connectivity between rSMG and medial cingulate cortex.