Autistic Syndrome Modulates Interpersonal Neural Synchronization in Children with Autism Spectrum Disorder in Cooperative Interactions

Background: The core symptom of individuals with autism spectrum disorder (ASD) includes social deficits in communication and interpersonal interaction. However, most neuroscience studies exploring the neural subtracts of the social deficits in ASD have mainly examined single participants’ brain responses to pictures or video-clips displayed on a monitor from a perspective of a passive observer, due to the limitation of the brain-imaging technique.

Objectives: Our goal was to fully understand the neural processing in children with ASD during real interpersonal interactions. Especially, we wanted to test whether interactive cooperation behaviors could evoke higher interpersonal neural coherence (INC) than solo, non-interactive behaviors in children with ASD, as previously found in typically-developing individuals (e.g., Cui et al., 2012). Furthermore, we aimed to examine whether the degree of the synchronization was modulated by the severity of autistic syndrome in children with ASD.

Methods: We used a functional near-infrared spectroscopy (fNIRS) based hyper-scanning technique to simultaneously measure the prefrontal activations in 15 pairs of children with ASD (6- to 11-year-old) and their parents in a two-person key-press task. The children's task was to press a key when a “go” signal was present to show synchronized behavior with their parents in a cooperation condition or to press a key as fast as possible under observation of their parents in a single condition. We also measured these children’s severity of autistic syndrome using the autism spectrum quotient (AQ).

Results: Behavioral results were shown in Figure 1. Children showed worse performance in the cooperation condition than in the single condition. Additionally, we found positive correlations between DRT (difference of response time between the children and their parents in the cooperation condition) and AQ communication and imagination subscale scores, indicating that children with ASD with higher levels of autistic syndrome had lower action synchronization with their parents.Concerning the neural results (Figure 2), the child-parent pairs showed higher INC across their right superior frontal cortex (SFC) in the cooperation condition than in the single condition. Importantly, there were negative correlations between DINC (difference of INC between the single and cooperation conditions) and AQ communication, imagination subscale and total scores. That means children with ASD with higher levels of autistic syndrome showed less increased neural synchronization with their parents when they were engaged in interactive cooperation behaviors than in solo, non-interactive behaviors. In addition, we found a negative correlation between DRT and DINC.

Conclusions: The present study examined inter-brain communication between children with ASD and their parents in real social interactions. We found that children with ASD showed increased interpersonal neural synchronization in the right SFC in the cooperative interactions with their parents than their solo, non-interactive behaviors. Furthermore, this neural synchronization was modulated by the children’s autistic syndrome, which also covaried with their cooperation task performance. Our study moved a major step forward to understanding of neural correlates underlying social deficits in ASD.