Caregiver-child interaction as an effective tool for identifying autism spectrum disorder: evidence from EEG analysis

Abstract

Background: Autism Spectrum Disorder (ASD) is a complex neurodevelopmental disorder that affects individuals across their lifespan. Early diagnosis and intervention are crucial for improving outcomes. However, current diagnostic methods are often time-consuming, and costly, making them inaccessible to many families. In the current study, we aim to test caregiver-child interaction as a potential tool for screening children with ASD in clinic.

Methods: We enrolled 85 preschool children (Mean age: 4.90 ± 0.65 years, 70.6% male), including ASD children with or without developmental delay (DD), and typical development (TD) children, along with their caregivers. ASD core symptoms were evaluated by Childhood Autism Rating Scale (CARS) and Autism Diagnostic Observation Schedule-Calibrated Severity Scores (ADOS-CSS). Behavioral indicators were derived from video encoding of caregiver-child interaction, including social involvement of children (SIC), interaction time (IT), response of children to social cues (RSC), time for caregiver initiated social interactions (GIS) and time for children initiated social interactions (CIS)). Power spectral density (PSD) values were calculated by EEG signals simultaneously recorded. Partial Pearson correlation analysis was used in both ASD groups to investigate the correlation among behavioral indicators scores and ASD symptom severity and PSD values. Receiver operating characteristic (ROC) analysis was used to describe the discrimination accuracy of behavioral indicators.

Results: Compared to TD group, both ASD groups demonstrated significant lower scores of SIC, IT, RSC, CIS (all p values < 0.05), and significant higher time for GIS (all p values < 0.01). SIC scores negatively correlated with CARS (p = 0.006) and ADOS-CSS (p = 0.023) in the ASD with DD group. Compared to TD group, PSD values elevated in ASD groups (all p values < 0.05), and was associated with SIC (theta band: p = 0.005; alpha band: p = 0.003) but not IQ levels. SIC was effective in identifying both ASD groups (sensitivity/specificity: ASD children with DD, 76.5%/66.7%; ASD children without DD, 82.6%/82.2%).

Conclusion: Our results verified the behavioral paradigm of caregiver-child interaction as an efficient tool for early ASD screening.

Keywords: Autism spectrum disorder; Caregiver-child interaction; Electroencephalography; Social interaction.

Fig. 1

Study flowchart. (A) All participants engaged in a 3–5 min free play session face-to-face with their caregiver, while simultaneously collecting video and EEG signals. (B) After offline coding of the interaction video and preprocessing of EEG data, indicators were calculated and statistical analysis was performed. (C) After preprocessing the EEG data, PSD (power spectral density) values were obtained through FFT transformation in theta and alpha bands

Fig. 2

Comparison of behavioral coding indicators among ASD with DD, ASD without DD, and TD children. (A) Differences in Social Involvement of Children (SIC) among the three groups. (B) Differences in Interaction Time (IT) among the three groups. (C) Differences in Responding to Social Cues (RSC) among the three groups. (D) Differences in caregivers Initiated Social interaction (GIS) among the three groups. (E) Differences in children Initiated Social interaction (CIS) among the three groups. The standard error of the mean is displayed as error bars. Significant differences between groups are indicated by horizontal bars and statistical significance is denoted by asterisks (*, p < 0.05; **, p < 0.01; ***, p < 0.001). ASD with DD, Autism disorder spectrum children with development delay group; ASD without DD, Autism disorder spectrum children without development delay group; TD, typical development children group

Fig. 3

Scatterplots depicting the associations between symptom severity and SIC within each group. (A) Correlations between SIC and Childhood Autism Rating Scale (CARS) (B) Correlations between SIC and the social impairment subscale of CARS. (C) The correlations between SIC and the Autism Diagnostic Observation Schedule- Calibrated Severity Score (ADOS-CSS). For test statistics, see Table S2. ASD with DD, Autism disorder spectrum children with development delay group; ASD without DD, Autism disorder spectrum children without development delay group; TD, typical development children group; OVERALL, full sample

Fig. 4

The differences in AUC analyze of behavioral indicators and PSD values in 3 groups. (A) The ROC curve of 5 behavioral indicators differentiating ASD children (with or without DD) from TD children. (B) The ROC curve of 5 behavioral indicators differentiating ASD children without DD from TD children. (C) The ROC curve of 5 behavioral indicators differentiating ASD children with DD from TD children. Abbreviations: ROC, receiver operating characteristic; AUC, area under the receiver operating curve; ASD, autism spectrum disorder; DD, developmental delay; TD, typically development; SIC, Social Involvement of Children; IT, Interaction Time; RSC, Response of children to Social Cues; GIS, Caregiver Initiated Social interaction; CIS, Children Initiated Social interactions

Fig. 5

The differences in alpha PSD between the ASD and TD groups. (A) The alpha PSD of children in three groups. (B) Correlations between verbal IQ and PSD. (C) Correlations between verbal IQ and PSD residuals following partial SIC (i.e., correlation between residuals). (D) Correlation between the SIC and alpha band’s PSD. (E) Correlation between the residuals for the SIC and alpha PSD following the partial elimination of verbal IQ (i.e., correlation between residuals). Within each diagnostic group and for the whole sample, correlation lines are displayed. For test statistics, see Table 3. The standard error of the mean is displayed as error bars. Significant changes between conditions are indicated by horizontal bars and * (*, p < 0.05; **, p < 0.01; ***, p < 0.001. The p values weren’t adjusted for multiple comparison (Bonferroni)). ASD with DD, Autism disorder spectrum children with development delay group; ASD without DD, Autism disorder spectrum children without development delay group; TD, typical development children group