Activation of the left medial temporal gyrus and adjacent brain areas during affective theory of mind processing correlates with trait schizotypy in a nonclinical population

Abstract

Schizophrenia, a severe psychiatric disorder, is associated with abnormal brain activation during theory of mind (ToM) processing. Researchers recently suggested that there is a continuum running from subclinical schizotypal personality traits to fully expressed schizophrenia symptoms. Nevertheless, it remains unclear whether schizotypal personality traits in a nonclinical population are associated with atypical brain activation during ToM tasks. Our aim was to investigate correlations between fMRI brain activation during affective ToM (ToMA) and cognitive ToM (ToMC) tasks and scores on the Schizotypal Personality Questionnaire (SPQ) and the Basic Empathy Scale in 39 healthy individuals. The total SPQ score positively correlated with brain activation during ToMA processing in clusters extending from the left medial temporal gyrus (MTG), lingual gyrus and fusiform gyrus to the parahippocampal gyrus (Brodmann area: 19). During ToMA processing, the right inferior occipital gyrus, right MTG, precuneus and posterior cingulate cortex negatively correlated with the emotional disconnection subscore and the total score of self-reported empathy. These posterior brain regions are known to be involved in memory and language, as well as in creative reasoning, in nonclinical individuals. Our findings highlight changes in brain processing associated with trait schizotypy in nonclinical individuals during ToMA but not ToMC processing.

Keywords: CHR; fMRI; psychosis proneness; schizophrenia; schizotypy; social cognition.

Fig. 1.

Brain activation related to the experimental task in four contrasts of interest. (A) Main effect of ToMA and ToMC relative to PC in healthy participants. Overlapping activation was observed in the precuneus. ToMA activation was widely distributed and concerned the mPFC, precuneus/PCC, superior temporal gyrus and temporoparietal junction, MTG, anterior cingulate cortex and inferior frontal gyrus. (B) The comparison between ToMA and ToMC showed that ToMA elicited the anterior part of the mPFC and the posterior cingulate (not shown), while ToMC relied on posterior brain regions (i.e. lingual and fusiform gyri). P < 0.05 FWE-corrected, k = 20.

Fig. 2.

The ToMA > PC contrast of brain activation when the total SPQ was modeled as a covariate revealed a positive correlation between the total SPQ and the left posterior brain regions, namely fusiform, calcarine et parahippocampal gyrus and, in lesser extent, activation was observed in the right calcarine and lingual gyrus. On the left, oblique posterior view on the 3D reconstruction. P < 0.001 uncorrected, k = 20.

Fig. 3.

Scatter plots of significant correlations between brain activation regions for the SPQ clinical score and subscores. Brain coordinates are reported in the MNI system. In ToMA > PC contrast, we found a positive correlation between the left MTG activation and the SPQ total score (A), and positive (C) and negative (D) subscores. In ToMC > ToMA contrast, a negative correlation between the left lingual gyrus activation and the positive SPQ subscore is represented (B).

Fig. 4.

Scatter plots of significant correlations between brain activation regions for the BES clinical score and subscores. Brain coordinates are reported in the MNI system. In ToMA > PC contrast, we found a positive correlation between the total BES score and the right MTG (A), and precuneus (B). Emotional disconnection clinical subscore correlated negatively to the right IOG in ToMA > PC contrast (C) and to the PCC in ToMA > ToMC contrast (D).