Abstract

Both schizophrenia (SCZ) and autism spectrum disorder (ASD) are characterized by mentalizing problems and associated neural dysfunction of the social brain. However, the deficits in mental state attribution are somehow opposed: Whereas patients with SCZ tend to over-attribute intentions to agents and physical events ("hyper-intentionality"), patients with autism treat people as devoid of intentions ("hypo-intentionality"). Here we aimed to investigate whether this hypo-hyper-intentionality hypothesis can be supported by neural evidence during a mentalizing task. Using functional magnetic resonance imaging (fMRI), we investigated the neural responses and functional connectivity during reading others intention. Scanning was performed in 23 individuals with ASD, 18 with paranoid SCZ and 23 gender and IQ matched control subjects. Both clinical groups showed reduced brain activation compared to controls for the contrast intentional vs physical information processing in left posterior superior temporal sulcus (pSTS) and ventral medial prefrontal cortex (vMPFC) for SCZ, and right pSTS in ASD. As predicted, these effects were caused in a group specific way: Relative increased activation for physical information processing in SCZ that was also correlated with positive PANNS score and relative decreased activation for intentional information processing in ASD. Additionally, we could demonstrate opposed connectivity patterns between the right pSTS and vMPFC in the clinical groups, ie, increased for SCZ, decreased for ASD. These findings represent opposed neural signatures in key regions of the social brain as predicted by the hyper-hypo-intentionality hypothesis.

Highlights

  • Autism spectrum disorder (ASD) and schizophrenia (SCZ) are 2 distinct neuropsychiatric disorders: ASD is characterized by deficits in social communication alongside stereotyped, repetitive behaviors,[1] whereas SCZ is characterized by a combination of positive and negative symptoms.[2]

  • When comparing each intentional condition (PInt and Communicative intention (CInt)) with the physical control condition (PhC), differences in activation patterns between groups were found driven by specific aberrant activation within the 4 region of interest (ROI) in pair-wise comparisons as predicted

  • For CInt>PhC, the TD group compared to the SCZ group showed higher activation in the left posterior superior temporal sulcus (pSTS) and ventral medial prefrontal cortex (MPFC)

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Summary

Introduction

Autism spectrum disorder (ASD) and schizophrenia (SCZ) are 2 distinct neuropsychiatric disorders: ASD is characterized by deficits in social communication alongside stereotyped, repetitive behaviors,[1] whereas SCZ is characterized by a combination of positive (hallucinations, delusions, and thought disorder) and negative symptoms (apathy, speech impairment, and flat affect).[2]. Social cognition refers to automatic and controlled psychological processes that support social interaction.[4] In particular, a specific cognitive ability, referred to as “theory of mind” (ToM), mentalizing or mind-reading, allows humans to represent and attribute different types of mental states to others, ie, inferring beliefs and reading intentions. The medial prefrontal cortex (MPFC) and the right posterior superior temporal sulcus (pSTS) along with the adjacent temporo-parietal junction (TPJ) are prominently involved in intention reading[5,6,7]: The MPFC is activated in social situations, implying communicative intent and triadic social interaction,[5,7] whereas the right pSTS/TPJ is engaged in processing more basic and simple intentions like recognizing a person’s goal.[7]. In ASD, reduced activation during processing of social information has been described in the right pSTS,[21,22,23,24] as well as decreased fronto-temporal connectivity during mind-reading.[25]

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