Cortical signatures of auditory object binding in children with autism spectrum disorder are anomalous in concordance with behavior and diagnosis

• Published in: PLoS biology 2022-02, Vol.20 (2), p.e3001541-e3001541
• Main Authors: Bharadwaj, Hari, Mamashli, Fahimeh, Khan, Sheraz, Singh, Ravinderjit, Joseph, Robert M, Losh, Ainsley, Pawlyszyn, Stephanie, McGuiggan, Nicole M, Graham, Steven, Hämäläinen, Matti S, Kenet, Tal
• Format: Article
• Language: English
• Subjects: Abnormalities; Auditory stimuli; Autism; Autistic children; Behavior; Biology and Life Sciences; Cerebrum; Children; Coherence; Demographic aspects; Diagnosis; Health aspects; Hearing; Hypotheses; Information processing; Magnetoencephalography; Medicine and Health Sciences; Object recognition; Patient outcomes; Pervasive developmental disorders; Physiological aspects; Psychological aspects; Research and Analysis Methods; Scene analysis; Short Reports; Social Sciences; Sound sources
• ISSN: 1545-7885; 1544-9173; 1545-7885
• DOI: 10.1371/journal.pbio.3001541

Organizing sensory information into coherent perceptual objects is fundamental to everyday perception and communication. In the visual domain, indirect evidence from cortical responses suggests that children with autism spectrum disorder (ASD) have anomalous figure-ground segregation. While auditory processing abnormalities are common in ASD, especially in environments with multiple sound sources, to date, the question of scene segregation in ASD has not been directly investigated in audition. Using magnetoencephalography, we measured cortical responses to unattended (passively experienced) auditory stimuli while parametrically manipulating the degree of temporal coherence that facilitates auditory figure-ground segregation. Results from 21 children with ASD (aged 7-17 years) and 26 age- and IQ-matched typically developing children provide evidence that children with ASD show anomalous growth of cortical neural responses with increasing temporal coherence of the auditory figure. The documented neurophysiological abnormalities did not depend on age, and were reflected both in the response evoked by changes in temporal coherence of the auditory scene and in the associated induced gamma rhythms. Furthermore, the individual neural measures were predictive of diagnosis (83% accuracy) and also correlated with behavioral measures of ASD severity and auditory processing abnormalities. These findings offer new insight into the neural mechanisms underlying auditory perceptual deficits and sensory overload in ASD, and suggest that temporal-coherence-based auditory scene analysis and suprathreshold processing of coherent auditory objects may be atypical in ASD.