Reduced Neural Activity in the Action Observation and Mentalizing Network in Children and Adolescents with Autism Spectrum Disorder during Execution, Imitation and Mentalization of Social and Motor Actions

Background: A growing body of literature suggests that children with ASD often have motor deficits and that these deficits may be related to social skills in ASD (Dziuk, 2007). Previous imaging work has shown that motor system networks (e.g., Action Observation Network (AON)) play a role in supporting intention understanding as well as imitation (Iacoboni, 2005). It is thus possible that mechanisms underlying motor impairments contribute to social deficits in ASD. To our knowledge, no study to date has investigated social and motor neural processing in ASD across a spectrum of social-motor stimuli.

Objectives: (1) To assess neural differences in children with and without ASD while they observe, execute, imitate and mentalize social and motor actions. (2) To assess how these differences may be related to group differences in social and motor skills assessed with the Social Responsiveness Scale (SRS; Constantino, 2003) and the Sensory Integration and Praxis Test (SIPT; Ayres, 1988).

Methods: Six high-functioning children and adolescents with ASD (mean age [years] 11.26±1.09) and ten typically developing (TD) participants (mean age [years] 11.25±1.41) were recruited. Imaging data was collected on a 3-T Siemens MAGNETOM Prisma scanner. The imaging protocol included a T1-weighted structural and standard EPI scans. In the scanner, participants observed, executed, imitated and mentalized separately to three video stimuli conditions: (1) emotional expressions (i.e., Happy), (2) Non-Emotional expressions (i.e., wiggle nose) and (3) hand actions (i.e., cutting paper). Using a block design, each condition was randomly presented for 15-seconds followed by 15-seconds of rest. Standard preprocessing and motion scrubbing were performed. Direct comparisons between groups were made in regions of the AON (i.e., Inferior frontal gyrus; IFG). The degree of social and motor skills was analyzed to determine group differences in ability.

Results: TD and ASD groups showed no group differences in AON activation when observing social and motor actions. However, during the motor action tasks, the ASD group showed reduced activity in IFG compared to the TD group (bilateral during execution and left lateralized during imitation (p<.054)). During mentalizing, ASD participants showed decreased recruitment of action understanding regions; the left IFG (p<.039) and temporal parietal junction (TPJ; p<.078) when processing the most novel stimuli (non-emotional faces) and the most social stimuli (emotional faces), respectively. Groups differed behaviorally in motor (p<.002) and social skills (p<.001).

Conclusions: Our results support previous findings of behavioral and neural motor processing deficits in ASD. Specifically, these data suggest an impairment in the AON which may be related to sensory-motor mapping in the IFG. Differences observed in the hand conditions may be driven by the execution of hand actions since group differences were not seen during observation of the actions alone. Our mentalizing findings concord with the theory that left IFG activation during mentalizing may underlie communication disorders in ASD (Kleinhas, 2008) and TPJ activation with more social processing deficits. Ongoing analysis will continue to investigate these findings and make direct comparisons of brain function and behavioral characteristics associated with the AON.