Neural responsivity to social rewards in autistic female youth
Katherine E. Lawrence, Leanna M. Hernandez, Jeffrey Eilbott, Allison Jack, Elizabeth Aylward, Nadine Gaab, John D. Van Horn, Raphael Bernier, Daniel H. Geschwind, James C. McPartland, Charles A. Nelson, Sara Jane Webb, Kevin A. Pelphrey, Susan Y. Bookheimer, Mirella Dapretto, Elizabeth Aylward, Raphael Bernier, Susan Y. Bookheimer, Mirella Dapretto, Nadine Gaab, Daniel H. Geschwind, Allison Jack, James C. McPartland, Charles A. Nelson, Kevin A. Pelphrey, John D. Van Horn, Sara Jane Webb, Katy Ankenman, Sarah Corrigan, Dianna Depedro-Mercier, Desiree Guilford, Abha R. Gupta, Zachary Jacokes, Shafali Jeste, Cara M. Keifer, Anna Kresse, Erin J. Libsack, Jennifer K. Lowe, Erin MacDonnell, Nicole M. McDonald, Adam Naples, Emily Neuhaus, Catherine Sullivan, Heidi Tsapelas, Carinna M. Torgerson, Pamela Ventola, Olivia Welker, Julie M. Wolf
Abstract
Autism is hypothesized to be in part driven by a reduced sensitivity to the inherently rewarding nature of social stimuli. Previous neuroimaging studies have indicated that autistic males do indeed display reduced neural activity to social rewards, but it is unknown whether this finding extends to autistic females, particularly as behavioral evidence suggests that affected females may not exhibit the same reduction in social motivation as their male peers. We therefore used functional magnetic resonance imaging to examine social reward processing during an instrumental implicit learning task in 154 children and adolescents (ages 8-17): 39 autistic girls, 43 autistic boys, 33 typically developing girls, and 39 typically developing boys. We found that autistic girls displayed increased activity to socially rewarding stimuli, including greater activity in the nucleus accumbens relative to autistic boys, as well as greater activity in lateral frontal cortices and the anterior insula compared with typically developing girls. These results demonstrate for the first time that autistic girls do not exhibit the same reduction in activity within social reward systems as autistic boys. Instead, autistic girls display increased neural activation to such stimuli in areas related to reward processing and salience detection. Our findings indicate that a reduced sensitivity to social rewards, as assessed with a rewarded instrumental implicit learning task, does not generalize to affected female youth and highlight the importance of studying potential sex differences in autism to improve our understanding of the condition and its heterogeneity.