Greater Social Competence Is Associated With Higher Interpersonal Neural Synchrony in Adolescents With Autism

Abstract

Difficulty engaging in reciprocal social interactions is a core characteristic of autism spectrum disorder. The mechanisms supporting effective dynamic real-time social exchanges are not yet well understood. This proof-of-concept hyperscanning electroencephalography study examined neural synchrony as the mechanism supporting interpersonal social interaction in 34 adolescents with autism spectrum disorder (50% female), age 10–16 years, paired with neurotypical confederates of similar age. The degree of brain-to-brain neural synchrony was quantified at temporo-parietal scalp locations as the circular correlation of oscillatory amplitudes in theta, alpha, and beta frequency bands while the participants engaged in a friendly conversation. In line with the hypotheses, interpersonal neural synchrony was significantly greater during the social interaction compared to the baseline. Lower levels of synchrony were associated with increased behavioral symptoms of social difficulties. With regard to sex differences, we found evidence for stronger interpersonal neural synchrony during conversation than baseline in females with autism, but not in male participants, for whom such condition differences did not reach statistical significance. This study established the feasibility of hyperscanning during real-time social interactions as an informative approach to examine social competence in autism, demonstrated that neural coordination of activity between the interacting brains may contribute to social behavior, and offered new insights into sex-related variability in social functioning in individuals with autism spectrum disorders.

Translational Applications of Neuroimaging

“…Quiñones-Camacho et al (2021) on the other hand, reported that healthy adults showed more neural synchrony than participants with ASD in the TPJ during a conversation task in an fNIRS study. Similarly, Key et al (2022) reported that in typically developing adolescents and in adolescents with ASD, lower levels of synchrony, as measured with EEG, were associated with increased behavioral symptoms of social difficulties. Furthermore, Tanabe et al (2012) used a real-time jointattention task combined with dual-fMRI recordings and found that detecting gaze direction was impaired in both healthy subjects and subjects with ASD, when they were paired together and inter-brain coherence in the right inferior frontal gyrus (IFG) together with intrabrain functional connectivity between the right IFG and right superior temporal sulcus (STS) was diminished in ASD.…”

“…In line with, a growing number of studies investigated interpersonal synchrony in ASD, and more recently also focused on INS (e.g., Lyons et al, 2020;Kruppa et al, 2021;Quiñones-Camacho et al, 2021;Key et al, 2022). Since these studies vary tremendously in the participants' age (children, adolescents, and adults), as well as in tasks and imaging techniques (EEG, fMRI and fNIRS), it is difficult at this point to draw any strong conclusions.…”

Interpersonal Neural Synchrony and Mental Disorders: Unlocking Potential Pathways for Clinical Interventions

“…Quiñones-Camacho et al ( 2021) on the other hand, reported that healthy adults showed more neural synchrony than participants with ASD in the TPJ during a conversation task in an fNIRS study. Similarly, Key et al (2022) reported that in typically developing adolescents and in adolescents with ASD, lower levels of synchrony, as measured with EEG, were associated with increased behavioral symptoms of social difficulties. Furthermore, Tanabe et al (2012) used a real-time jointattention task combined with dual-fMRI recordings and found that detecting gaze direction was impaired in both normal subjects and subjects with ASD, when they were paired together and interbrain coherence in the right inferior frontal gyrus (IFG) together with intra-brain functional connectivity between the right IFG and right superior temporal sulcus (STS) was diminished in ASD.…”

Interpersonal neural synchrony and mental disorders: unlocking potential pathways for clinical interventions

“…In line with, a growing number of studies investigated interpersonal synchrony in ASD, and more recently also focused on INS (e.g., Lyons et al, 2020;Kruppa et al, 2021;Quiñones-Camacho et al, 2021;Wang et al, 2021;Key et al, 2022). Since these studies vary tremendously in the participants' age (children, adolescents, and adults), as well as in tasks and imaging techniques (EEG, fMRI and fNIRS), it is difficult at this point to draw any strong conclusions.…”