Atypical frontal-posterior synchronization of Theory of Mind regions in autism during mental state attribution

Abstract

This study used fMRI to investigate the functioning of the Theory of Mind (ToM) cortical network in autism during the viewing of animations that in some conditions entailed the attribution of a mental state to animated geometric figures. At the cortical level, mentalizing (attribution of metal states) is underpinned by the coordination and integration of the components of the ToM network, which include the medial frontal gyrus, the anterior paracingulate, and the right temporoparietal junction. The pivotal new finding was a functional underconnectivity (a lower degree of synchronization) in autism, especially in the connections between frontal and posterior areas during the attribution of mental states. In addition, the frontal ToM regions activated less in participants with autism relative to control participants. In the autism group, an independent psychometric assessment of ToM ability and the activation in the right temporoparietal junction were reliably correlated. The results together provide new evidence for the biological basis of atypical processing of ToM in autism, implicating the underconnectivity between frontal regions and more posterior areas.

Keywords:

• Autism
• Mentalizing
• Theory of Mind (ToM)
• Mental state
• fMRI
• Underconnectivity

Acknowledgements

This research was supported by Collaborative Program of Excellence in Autism (CPEA) Grant HD35469 from the National Institute of Child Health and Human Development and the Cure Autism Now Young Investigator Award to Rajesh K. Kana. The authors thank Fulvia Castelli (King's College, London, UK) for generously providing the animation stimuli for our study. The authors also thank Diane Williams for her assistance in collecting the ToM scores, Sarah Schipul and Stacey Becker for assistance with the data collection and data analysis, and Rachel Krishnaswami for editorial comments on an earlier version of the manuscript.