Markers for the central serotonin system correlate to verbal ability and paralinguistic social voice processing in autism spectrum disorder

Yuko Yoshimura,Hirotaka Kosaka,Tetsuya Takahashi,Yasuomi Ouchi,Yoshio Minabe,Mitsuru Kikuchi,Tetsu Hirosawa,Toshio Munesue,Nobushige Naito,Daisuke N Saito

doi:10.1038/s41598-020-71254-w

Yuko Yoshimura, Hirotaka Kosaka + Show 8 more

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https://doi.org/10.1038/s41598-020-71254-w

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Impairment in verbal communication abilities has been reported in autism spectrum disorder (ASD). Dysfunction of the serotonergic system has also been reported in ASD. However, it is still unknown how the brain serotonergic system relates to impairment in verbal communication abilities in individuals with ASD. In the present study, we investigated the correlation between brain serotonergic condition and brain sensitivity to paralinguistic stimuli (i.e., amplitude in the human voice prosodic change-evoked mismatch field) measured by magnetoencephalography (MEG) or verbal ability in 10 adults with ASD. To estimate the brain serotonergic condition, we measured the serotonin transporter nondisplaceable binding potential cerebrum-wide using positron emission tomography with [11C]N,N-dimethyl-2-(2-amino-4-cyanophenylthio)benzylamine ([11C] DASB). The results demonstrated a significant positive correlation between brain activity to paralinguistic stimuli and brain serotonin transporter binding potential in the left lingual gyrus, left fusiform gyrus and left calcarine cortex. In addition, there were significant positive correlations between verbal ability and serotonergic condition in the right anterior insula, right putamen and right central operculum. These results suggested that the occipital cortex is implicated in recognition of the prosodic change in ASD, whereas the right insula-involved serotonergic system is important in nurturing verbal function in ASD.Trial registration: UMIN000011077.

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Impairment in verbal communication abilities has been reported in autism spectrum disorder (ASD)
We selected the superior temporal lobe and the banks of the superior temporal sulcus as regions of interest (ROIs) based on the prediction that mismatch field (MMF) generators would be located primarily in the superior temporal regions[15,39,40,41,42]
In the left lingual gyrus (r = 0.94, P < 0.001, uncorrected for the peak voxel), left fusiform gyrus (r = 0.95, P < 0.001, uncorrected for the peak voxel) and left calcarine cortex (r = 0.95, P < 0.001, uncorrected for the peak voxel) (P < 0.05, family wise error corrected for cluster size with a height threshold of P < 0.001) (Table 1, Fig. 1), statistical parametric mapping (SPM) demonstrated that serotonin transporter (SERT) B PND are positively correlated with MMF intensity evoked in the right superior temporal area

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Introduction

Impairment in verbal communication abilities has been reported in autism spectrum disorder (ASD). Dysfunction of the serotonergic system has been reported in ASD It is still unknown how the brain serotonergic system relates to impairment in verbal communication abilities in individuals with ASD. To estimate the brain serotonergic condition, we measured the serotonin transporter nondisplaceable binding potential cerebrum-wide using positron emission tomography with [11C] N,N-dimethyl-2-(2-amino-4-cyanophenylthio)benzylamine ([11C] DASB). Abbreviations ASD Autism spectrum disorder SERT Serotonin transporter SSRIs Selective serotonin reuptake inhibitors PET Positron emission tomography BPND Binding potential MMN Mismatch negativity MMF Mismatch field. In adults with ASD, PET studies have demonstrated decreases in the level of SERT binding potential (BPND) throughout the brain, with SERT BPND reduction in the anterior and posterior cingulate cortices being linked to impairment of social c ognition[6].

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