Neural Responsivity to Social Rewards and Mirror Neuron System Activity in Children with and without Autism

Background:

The social motivation hypothesis posits that children with autism spend less time attending to faces and other social stimuli, thus leading to a cascade of negative consequences for the development of social cognition (Dawson et al., 1998; Grelotti et al., 2002). This reduced social motivation is thought to result from a failure to attach a reward value to social stimuli early in development. It has also been proposed that a dysfunctional ‘mirror neuron system’ (MNS) may give rise to the social impairments that are characteristic of autism (Ramachandran, 2000). The MNS is thought to constitute a neural substrate for automatically understanding others via a simulation mechanism (Rizzolatti & Fabbri-Destro, 2008). The normal functioning of this system may code the ‘like me’ analogy between self and others (Gallese, 2003) perhaps contributing to the attentional biases toward social stimuli observed during typical development. MNS abnormalities in autism may alter this developmental trajectory as children with autism may not find social stimuli rewarding if they fail to grasp this self/other equivalence which is fundamental for the development of social cognition (Meltzoff, 2007).
Objectives:

The aim of this study was to examine the relationship between reward-related activity in the ventral striatum (VS) and activity in frontal regions such as the inferior frontal gyrus (IFG) during a socially rewarded learning task in children with and without autism spectrum disorders (ASD).
Methods:

16 boys with ASD (12.4 + 2.14 years) and 16 age- and IQ-matched typically developing (TD) boys were scanned during a socially rewarded implicit learning task. Region-of-interest (ROI) analyses were conducted within the right pars opercularis (PrOp) of the IFG and a functionally defined ROI within the VS. Within-group bivariate correlations were conducted on percent signal change within the PrOp and VS during social feedback events. A multiple linear regression on PrOp activity across groups was also conducted. 
Results:

We found significant positive correlations between activity in the VS and activity in the right PrOp (BA 44) for TD children. Specifically, we found that VS response to positive social feedback significantly correlated with both positive (r = 0.824, p < 0.001) and negative (r = 0.714, p < 0.001) emotional facial feedback compared to rest, but not with neutral expression positive feedback compared to rest (TD: r = -0.31, p = 0.245; ASD: r = -0.21, p = 0.435).No significant correlations for these two ROIs were observed within the ASD group. A multiple linear regression on PrOp activity with group, VS activity and group X VS interaction (F(3, 28) = 8.362, p < 0.001) revealed a significant interaction effect (b = 0.88; t = 2.17, p < 0.05). 
Conclusions:

We found evidence of strong functional connectivity between the right pars opercularis of the IFG and reward-related responses in VS in TD children for emotional social feedback. No such correlations were observed in children with ASD.  These findings support the social motivation hypothesis and provide evidence linking MNS dysfunction in autism to reward circuitry abnormalities in response to social stimuli.