Unique deficit in embodied simulation in autism: An fMRI study comparing autism and developmental coordination disorder

Abstract

A deficit in pre‐cognitively mirroring other people's actions and experiences may be related to the social impairments observed in autism spectrum disorder (ASD). However, it is unclear whether such embodied simulation deficits are unique to ASD or instead are related to motor impairment, which is commonly comorbid with ASD. Here we aim to disentangle how, neurologically, motor impairments contribute to simulation deficits and identify unique neural signatures of ASD. We compare children with ASD (N = 30) to children with Developmental Coordination Disorder (DCD; N = 23) as well as a typically developing group (N = 33) during fMRI tasks in which children observe, imitate, and mentalize about other people's actions. Results indicate a unique neural signature in ASD: during action observation, only the ASD group shows hypoactivity in a region important for simulation (inferior frontal gyrus, pars opercularis, IFGop). However, during a motor production task (imitation), the IFGop is hypoactive for both ASD and DCD groups. For all tasks, we find correlations across groups with motor ability, even after controlling for age, IQ, and social impairment. Conversely, across groups, mentalizing ability is correlated with activity in the dorsomedial prefrontal cortex when controlling for motor ability. These findings help identify the unique neurobiological basis of ASD for aspects of social processing. Furthermore, as no previous fMRI studies correlated brain activity with motor impairment in ASD, these findings help explain prior conflicting reports in these simulation networks.

Combined action observation and motor imagery: An intervention to combat the neural and behavioural deficits associated with developmental coordination disorder

“…Reduced BOLD activity has also been reported in both the left (Licari et al, 2015;Zwicker et al 2010) and right IFG (Debrabant et al, 2013;Kilroy et al, 2020;Reynolds et al, 2015b) in children with DCD. Bilaterally, the IFG is involved during MI, AO and action execution (Hardwick et al, 2018).…”

“…Furthermore, this would align with the recent call by Brown-Lum & Zwicker (2017) for mental training interventions to target supressed brain regions in children with DCD. Two AON regions reported to be impaired in this population are the precentral gyrus and pars opercularis of the IFG (Kilroy et al, 2020;Reynolds et al, 2015b). While the evidence for the suppression of these motor regions has only been obtained through AO and imitation in DCD (Reynolds et al, 2015b;2015a), these regions also play a role in MI and action execution in adults (Hardwick et al, 2018) and children (Reynolds et al, 2015b).…”

“…Within the IFG is the pars opercularis, a structure associated with imitation (Kilner et al, 2009;Molnar-Szakacs et al, 2005), MI generation and maintenance (Hétu et al, 2013), andAO (Molnar-Szakacs et al, 2005;Vogt et al, 2007). Region of interest analyses by Kilroy et al (2020) and Reynolds et al (2015b) revealed the pars opercularis of the right IFG to be activated less during imitation in this population. Studies by Nedelko et al (2012) and Taube et al (2015) found greater activations in the left and right IFG, respectively.…”

“…Reynolds et al (2019) found small group differences between children with and without DCD during imitation in regions associated with motor planning and motor attention, namely the thalamus, caudate, posterior cingulate cortex and the precuneus. A recent investigation of the AON in children with DCD by Kilroy et al (2020) found only significantly reduced activity within the pons during AO, but found significantly reduced activations during imitation tasks within the right IFG (pars opercularis), right superior frontal gyrus and the supplementary motor area. Using fMRI, Licari et al (2015) reported the left IFG to have reduced activation for children with DCD during an imitation task.…”

Sensory Modulation in Children with Developmental Coordination Disorder Compared to Autism Spectrum Disorder and Typically Developing Children

“…A total of 136 right-handed individuals aged 8–17 in either DCD ( N = 27; mean age = 11.75, SD = 2.31), ASD ( N = 57; mean age = 11.89, SD = 2.29), or TD ( N = 53; mean age = 11.75, SD = 2.13) groups completed the study. This study was part of a larger study that included brain imaging components, thus some inclusion criteria were based on those requirements [ 88 ]. Using the effect sizes from a meta-analysis on TD and ASD by Ben Sasson et al [ 89 ], we conducted a power analysis and found that the sample sizes we had were sufficient to achieve 97.5% power.…”