Tonotopic mapping in children shows an overrepresentation of high frequencies in autism

Abstract

Altered sensitivity to sounds despite normal peripheral hearing is common in neurodevelopmental disorders but the underlying mechanisms remain poorly understood. Here we investigate tonotopic organization in 86 children (6-11 years) with autism spectrum and related neurodevelopmental disorders as well as typically developing (TD) peers, using a child-friendly, passive listening, functional magnetic resonance imaging design. In TD children, tonotopic maps in primary auditory cortex resembled the typical high-low-high frequency gradients previously reported in adults, while children with autism showed an overrepresentation of high frequencies consistent with what has been observed in animal models of autism. Higher frequency tuning further correlated with greater caregiver-reported sound but not touch sensitivities. Importantly, tonotopy is a core organizational feature of auditory cortex that develops early in life and remains relatively stable after the critical period of heightened plasticity ends. Thus, these results suggest that atypical auditory processing in autism may result from early disruption to tonotopic map formation. Longitudinal neuroimaging studies are needed to understand the genetic and environmental causes of altered auditory cortex topology and its long-term consequences for higher-level auditory, language, and social communication development.