Reward System Response to Highly Salient Social Rewards In Autism

Background: The social motivation hypothesis (Dawson et al., 1998b, 2005; Schultz, 2005) of autism spectrum disorders (ASD) holds that social stimuli are not experienced as rewarding for children who later develop an ASD, and that this lack of reward leads to reduced social and affinitive behaviors and interests later in life. Recent neuroimaging work (Scott-Van Zeeland et al., 2010; Schmitz et al., 2008) has begun to focus on neural response to rewards in the canonical reward system which includes the ventral striatum (VS), subcallosal, anterior cingulate (ACC), and orbitofrontal (OfC) cortex.  Thus far, only one study (Scott-Van Zeeland et al., 2010) has tested the neurophysiological extension of the social motivation hypothesis finding hypoactivation of VS and thus supporting the social motivation hypothesis.  

Objectives: While VS hypoactivation to social rewards has been observed in adolescents with ASD, we aim to test whether the reward system in ASD is unresponsive to social rewards or whether the neural response to social rewards in ASD is circumscribed to highly salient social rewards.

Methods: We conducted an fMRI study with 21 (4 female) ASD and 19 (3 female) typically-developing (TD) participants who were equivalent on age, IQ, and head motion, using highly salient social rewards in the context of a modified Weather Prediction Task (WPT: Knowlton et al., 1994).  The task is a probabilistic learning paradigm where participants were presented abstract images and asked to respond as to whether a given picture is in group 1 or group 2. Pictures of the child’s primary caregiver, were used as the highly salient social stimuli.  Pictures of the mother were taken immediately before the fMRI study and incorporated into the program.  A smiling picture of the mother was shown after correct responses, and a “sad” or “disappointed” picture of the mother was shown after incorrect responses.  

Results: The TD group demonstrated greater VS and amygdala activation to the highly salient social rewards minus rest (fixation cross) compared to the ASD group while the ASD group demonstrated greater activation of subcallosal cortex and ACC than the TD group for this same contrast. 

Conclusions: These findings indicate that rather than being unresponsive to social rewards, when the social rewards are highly salient, children with ASD show what may be a compensatory pattern of activity in nodes of the reward system outside of the VS. The areas shown to be hypoactive in ASD are consistent with those reported by Scott-Van Zeeland et al (2010) in response to low salience social rewards vs. penalty (sad face).  Similarly, the areas showing hyperactivation in ASD are areas where Scott-Van Zeeland et al reported significant within group activation in the ASD group for social rewards vs. penalty. The present findings indicate that children with ASD do activate some nodes of the reward system; however, the pattern of activation is different than that observed in TD children and may represent neural compensation in regions activated for even low salience social rewards.