The Neural Basis of Action Understanding in Autism and Typical Development

Background:

In a social species, it is critical to understand the actions and intentions of others during interactions. In typically developing (TD) individuals, there are two neural systems that support action understanding of others: lower level motor simulation in the mirror system, and higher-level intention understanding in the mentalizing system. The fronto-parietal mirror system is active during both the observation and execution of motor actions (Molenberghs et al., 2011). The mentalizing system is engaged when reflecting about the desires or intentions of others (Blakemore et al., 2007), or when observing implausible actions (Buccino et al., 2007). These systems are rarely concurrently active, each working to support different aspects of action and intention understanding (Van Overwalle & Baetens, 2009). Individuals with autism spectrum disorders (ASD) generally have difficulty with understanding the actions and intentions of others (Happe & Frith, 1996; Williams et al., 2004). We sought to examine these systems in adolescents with and without ASD while they observed different types of actions (eating vs. placing). We examined differences in the neural responses when observing actions that differed in their motivation and intention – picking up an object to eat it or to place it elsewhere.

Objectives:

We examined the neural basis of action and intention understanding in ASD and TD using fMRI when observing eating and placing action sequences.

Methods:

Functional neuroimaging was obtained from age and gender matched children (aged 8-17 years) who were either TD or diagnosed with ASD. Participants passively viewed 4-second videos of conventional and unconventional eating or placing actions while functional images were acquired.

Results:

In the TD group, there was more activity in the mPFC, part of the mentalizing system, during the observation of eating than during placing. In ASD, no areas showed significantly greater activity during observation of eating compared to placing. While observing placing actions, greater than eating, both groups showed more activation in superior parietal areas, which is consistent with this area coding goal directed arm movements, as placing actions involved more arm movement than did eating. Additionally, in the ASD group there was greater activation to placing actions compared to eating in ventral premotor (vPM) cortex and the inferior parietal lobule, areas of the mirror system. Between the ASD and TD groups, the ASD group had significantly greater activity to placing then eating actions in vPM, along the STS, and in an area of the mPFC that is involved in mentalizing processes.

Conclusions:

The fMRI results suggest that the groups find different actions more salient, as areas of the mentalizing system were more active for eating in the TD group and for placing in the ASD group. Unexpectedly, the ASD group appeared to engage more mirror activation when observing placing actions, suggesting they are better able to simulate placing an object rather than eating. This may be related to individuals with ASD being preoccupied with objects and directing less attention toward other people and the actions they are performing, particularly those that are self-directed.