Neurodiversity in the brain: More variable localization of face regions in autism

Abstract A fundamental principle in human neuroscience is that the brain is organized into distinct functional regions specialized for particular processes. These functional regions develop early and are shaped by sensory experiences. Strikingly, the precise location of these functional regions is relatively consistent across individuals, with specific regions found in stereotyped locations with respect to the macroanatomy (e.g., particular sulci and gyri). An important question is how flexible this functional neuroanatomy is, particularly in neurodevelopmental disorders like autism which are characterized by atypical brain development and behavior. Here, we investigated this question by focusing on the organization of the face-processing network — a well-characterized system of regions that are reliably localized across neurotypical individuals, including, famously, the fusiform face area. Using precision fMRI, we identified subject-specific face-sensitive regions in the brains of autistic and neurotypical adults, and assessed their topographical alignment across individuals. Face regions in autism were globally and highly variably displaced – located farther from their expected locations in the brain relative to much more homogenous localization in neurotypical adults. Autistic individuals whose face regions were more displaced had greater sociocommunicative challenges. In contrast, the spatial organization of object-sensitive regions was not affected. These findings suggest that the spatial organization of the face network is atypical in autism, with behaviorally meaningful increased variability in the precise location of face-sensitive areas, and highlights the importance of individualized approaches in neuroimaging. Significance Statement The human brain is organized into specialized functional regions positioned in remarkably consistent locations across individuals. It is unclear how altered neurodevelopment affects this organization. Using precision fMRI, we found that autism was characterized by globally and highly variably displaced face-sensitive functional brain regions. Atypical spatial organization of these regions was associated with greater sociocommunicative difficulties. In contrast, the spatial organization of object-sensitive regions did not differ in autism. These findings reveal that functional neuroanatomy in autism is altered in category-specific ways, with direct relevance to core sociocommunicative features of the condition. This work underscores the importance of individualized brain mapping in neuroimaging and may shed light on inconsistent findings in previous group-level neuroimaging studies. Competing Interest Statement The authors have declared no competing interest. Footnotes Funding: AMO was supported by NIH awards T32-DC000038 and F31-DC020864 from the National Institute on Deafness and Other Communication Disorders (NIDCD), the Hock E. Tan and K. Lisa Yang Center for Autism Research, and a Simons Center for the Social Brain Postdoctoral Fellowship. TKP was supported by NIDCD R56-DC020208. AMD was supported by a Simons Center for the Social Brain Postdoctoral Fellowship and National Institute of Mental Health Postdoctoral Fellowship F32-MH117933. This work was also supported by the Simons Center for the Social Brain and the Hock E. Tan and K. Lisa Yang Center for Autism Research at the Massachusetts Institute of Technology.