Underconnectivity of the superior temporal sulcus predicts emotion recognition deficits in autism

Abstract

Neurodevelopmental disconnections have been assumed to cause behavioral alterations in autism spectrum disorders (ASDs). Here, we combined measurements of intrinsic functional connectivity (iFC) from resting-state functional magnetic resonance imaging (fMRI) with task-based fMRI to explore whether altered activity and/or iFC of the right posterior superior temporal sulcus (pSTS) mediates deficits in emotion recognition in ASD. Fifteen adults with ASD and 15 matched-controls underwent resting-state and task-based fMRI, during which participants discriminated emotional states from point light displays (PLDs). Intrinsic FC of the right pSTS was further examined using 584 (278 ASD/306 controls) resting-state data of the Autism Brain Imaging Data Exchange (ABIDE). Participants with ASD were less accurate than controls in recognizing emotional states from PLDs. Analyses revealed pronounced ASD-related reductions both in task-based activity and resting-state iFC of the right pSTS with fronto-parietal areas typically encompassing the action observation network (AON). Notably, pSTS-hypo-activity was related to pSTS-hypo-connectivity, and both measures were predictive of emotion recognition performance with each measure explaining a unique part of the variance. Analyses with the large independent ABIDE dataset replicated reductions in pSTS-iFC to fronto-parietal regions. These findings provide novel evidence that pSTS hypo-activity and hypo-connectivity with the fronto-parietal AON are linked to the social deficits characteristic of ASD.

Connectivity in Autism

“…20,22,29,33,39,40,47,49,50,55 Posterior cingulate cortex (PCC) was reported in eight studies to have reduced, 21,29–31,40,41,47,50 and in three reports to have increased, long-range connectivity to other ROIs. 30,41,43 The precuneus, 29,33,41,43,47,50 anterior cingulate cortex (ACC), 21,22,33,43,50 superior temporal gyrus, 34,39,43,50,54 posterior superior temporal sulcus, 20,49,53 anterior insula, 20,37,49 and parietal lobule 35,50,53,55 each had four to five reports of reduced, with either one or two reports of increased, long-range connectivities. Verly and colleagues 54 reported a widespread reduction in inter-hemispheric connectivity among the ROIs studied, with the exception of the arcuate fasciculus part of the superior longitudinal fasciculus).…”

“…33 Kewon and colleagues 56 reported a negative correlation between average local degrees of connectivity, the number of other regions to which the ROI connected, and social impairment (reported as a negative correlation with ADOS–Social Scale scores). The one outlier was a study by the Alaerts group, 53 which reported a positive correlation between RS connectivity involving posterior superior temporal sulcus seed and performance on the emotion-recognition task. The regions involved were the supplementary motor area, supramarginal gyrus, inferior frontal gyrus, and precentral gyrus.…”

Sex differences in autism: a resting-state fMRI investigation of functional brain connectivity in males and females

“…The STS coordinates were based on (Alaerts et al, 2014) and represent the STS region (right hemisphere) that was activated during an emotional processing task employing point light displays in young male adults with ASD and TC. The same STS seed previously exhibited reduced functional connectivity in males with ASD relative to TC (Alaerts et al, 2014).…”

“…Two hypothesis-driven connectivity measures were chosen based on prior reports of diagnosis-related alterations in males with ASD, which included (i) investigations of the functional circuitry of the posterior superior temporal sulcus (STS), a key 'hub' in social information processing by connecting distinct social brain networks underlying theory of mind (amygdala-orbitofrontal network) and action/emotion understanding (fronto-parietal action perception network or mirror neuron system) (Lahnakoski et al, 2012); and (ii) exploration of functional connections of the posterior cingulate cortex (PCC), a core region of the default network (Buckner et al, 2008), most prominently studied in prior ASD resting-state neuroimaging research. ASD-related alterations in functional circuitry have been reported for both regions in males with ASD (STS (Shih et al, 2010;Mueller et al, 2013;Alaerts et al, 2014); PCC (Cherkassky et al, 2006;Monk et al, 2009;Assaf et al, 2010;Weng et al, 2010)), and a key question will be whether and how these alterations are different in females with ASD.…”

Brain activity of adolescents with high functioning autism in response to emotional words and facial emoticons

“…Freitag et al [47] have suggested that the interpretation of complex motion may be associated with gray matter volumes within the right medial temporal cortex. Alaerts et al [48] reported that hypoactivity of posterior superior temporal sulcus might be linked with the social deficits characteristic of ASD patients. Herrington et al [49] reported that the detection of a point-light walking figure was associated with the activity within inferior frontal gyrus, fusiform gyrus, and amygdala.…”