Temporal and Spatial Neural Correlates of Theory of Mind in Children with ASD

Background: Theory of mind (ToM), or the ability to recognize the different mental states of others, is characteristically impaired in children with autism spectrum disorder (ASD), which is thought to contribute to their social cognitive deficits. Functional MRI studies have investigated the neural mechanisms underlying ToM, implicating the precuneus, temporoparietal junction (TPJ), and the medial prefrontal cortex (mPFC) as core regions of the ToM network. Studies in adults with ASD have shown atypical activation in these areas. However, only a few studies have examined the timing of brain activity during ToM reasoning, and none have explored this aspect in ASD, nor how it differs in children, even though deviations in the latency and duration of brain activity during development can also be responsible for the social impairments observed in ASD.

Objectives: This study determined the temporal and spatial properties of brain regions active during a false-belief ToM task in children with and without ASD using magnetoencephalography (MEG).

Methods: Participants included 22 typically-developing (TD) children and 19 age- and sex-matched children with ASD between the ages of 8 and 12 years. We studied the timing of ToM-related neural processes using a false-belief task adapted from Dennis et al. (2012) for MEG, which has precise temporal and spatial resolution on the order of milliseconds and millimetres, respectively. 

Results: While the two groups of children did not differ in performance on the false-belief task, whole-brain analyses revealed distinctive neural patterns. Whereas TD children activated familiar ToM regions, such as the right precuneus (150-225 ms and 325-400 ms) followed by the left TPJ (300-400 ms and 425-475 ms), children with ASD appeared to utilize verbal abilities to complete the same task, activating the left inferior frontal gyrus (IFG; 275-375 ms and 450-600 ms), while simultaneously relying on working memory, attention, and inhibition areas, such as the right dorsal TPJ overlapping with the right superior parietal lobule (275-375 ms and 450-600 ms) and the right IFG (300-600 ms).

Conclusions: Using MEG, we were able to detect a unique temporospatial recruitment of brain regions involved in understanding false belief in our participants with ASD, which suggests that children with ASD make use of alternative strategies to compensate for their deficits in ToM. As our group of children with ASD did not differ from controls on measures of working memory and inhibition, and given that the brain areas they activated are typically involved in these processes, these children may have employed these preserved executive functions to perform similarly to their peers on the ToM task. These results not only inform how ToM can be conserved in some children with high-functioning ASD, but they also demonstrate processes that could be harnessed in interventions to improve ToM and social cognition in children with ASD. Future work will expand our findings to the connectivity domain, as individuals with ASD have been shown to have atypical patterns of connectivity, and the interaction between executive functioning and ToM will be explored.