Abstract
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.
Highlights
Successful navigation of environments with multiple stimuli fundamentally relies on the brain’s ability to perceptually organize the barrage of sensory information into discrete coher-Grant, HB), Nancy Lurie Marks Family Foundation (TK), The Simons Foundation (SFARI 239395, TK), The National Institute of Child Health and Development (R01HD073254, TK), The National Institute of Mental Health (R01MH117998, R21MH116517, TK), National Institute for ently bound objects on which cognitive processes such as selective attention can act
This study aimed to test whether the cortical correlates of auditory figure–ground segregation based on temporal coherence may be abnormal in autism spectrum disorder (ASD)
We found that children with ASD had significantly attenuated evoked responses to the pop-out of the foreground figure, alongside a lower magnitude of induced gamma band activity
Summary
HB), Nancy Lurie Marks Family Foundation (TK), The Simons Foundation (SFARI 239395, TK), The National Institute of Child Health and Development (R01HD073254, TK), The National Institute of Mental Health (R01MH117998, R21MH116517, TK), National Institute for ently bound objects on which cognitive processes such as selective attention can act Failure of this scene-segregation process, where one source stands out as the foreground “figure” and the remaining stimuli form the “background,” can result in an overwhelming sensory experience that makes it difficult to select a source of interest while suppressing the others [1,2]. A leading hypothesis about sensory processing abnormalities in autism spectrum disorder (ASD) is that this kind of temporal “synthesis” of sensory information is atypical [5,6,7,8] This hypothesis stems from behavioral data indicating that individuals with ASD often show impaired processing of dynamic stimuli, such as the coherent motion of visual dots [9]. In the auditory domain, where stimuli are naturally dynamic, atypical sensory-stimu-
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