Reduced beta connectivity during emotional face processing in adolescents with autism

Abstract

BackgroundAutism spectrum disorder (ASD) is a neurodevelopmental disorder characterized by impairments in social cognition. The biological basis of deficits in social cognition in ASD, and their difficulty in processing emotional face information in particular, remains unclear. Atypical communication within and between brain regions has been reported in ASD. Interregional phase-locking is a neurophysiological mechanism mediating communication among brain areas and is understood to support cognitive functions. In the present study we investigated interregional magnetoencephalographic phase synchronization during the perception of emotional faces in adolescents with ASD.MethodsA total of 22 adolescents with ASD (18 males, mean age =14.2 ± 1.15 years, 22 right-handed) with mild to no cognitive delay and 17 healthy controls (14 males, mean age =14.4 ± 0.33 years, 16 right-handed) performed an implicit emotional processing task requiring perception of happy, angry and neutral faces while we recorded neuromagnetic signals. The faces were presented rapidly (80 ms duration) to the left or right of a central fixation cross and participants responded to a scrambled pattern that was presented concurrently on the opposite side of the fixation point. Task-dependent interregional phase-locking was calculated among source-resolved brain regions.ResultsTask-dependent increases in interregional beta synchronization were observed. Beta-band interregional phase-locking in adolescents with ASD was reduced, relative to controls, during the perception of angry faces in a distributed network involving the right fusiform gyrus and insula. No significant group differences were found for happy or neutral faces, or other analyzed frequency ranges. Significant reductions in task-dependent beta connectivity strength, clustering and eigenvector centrality (all P <0.001) in the right insula were found in adolescents with ASD, relative to controls.ConclusionsReduced beta synchronization may reflect inadequate recruitment of task-relevant networks during emotional face processing in ASD. The right insula, specifically, was a hub of reduced functional connectivity and may play a prominent role in the inability to effectively extract emotional information from faces. These findings suggest that functional disconnection in brain networks mediating emotional processes may contribute to deficits in social cognition in this population.Electronic supplementary materialThe online version of this article (doi:10.1186/2040-2392-5-51) contains supplementary material, which is available to authorized users.

Disconnection from others in autism is more than just a feeling: whole-brain neural synchrony in adults during implicit processing of emotional faces

“…Thus, hypo-connectivity in the left hemisphere during processing of angry faces supports the theory of poor motivation toward social stimuli in ASD compared to TD individuals [1–3]. Intriguingly, our findings largely overlap with results from Leung and colleagues who used the same task on adolescents with autism (range 12–15 years) [41]. Nonetheless, the latter study did not find the strong left lateralization for angry faces.…”

“…During processing of fearful and angry faces, reduced connectivity within the right fusiform gyrus and between the fusiform and the left precuneus, left inferior frontal gyrus and left anterior cingulate was reported in ASD, within 320 ms. In accordance with these results, decreased connectivity in beta band was also seen in adolescents with ASD during implicit processing of angry faces, in the first 400 ms after the stimuli [41]. In the latter study, reduced beta connectivity in ASD was anchored in connections between visual (e.g.…”

Development of Network Synchronization Predicts Language Abilities

“…This increased network synchronization strongly involved connectivity between areas of visual cortex and widespread areas of visual cortex, consistent with prior neuromagnetic studies of connectivity involving processing of a visual stimulus and using similar methods (i.e. Bangel et al, 2014;Leung et al, 2014) and encompassed brain areas including classic regions associated with language functions (i.e., Broca's and Wernicke's areas). Using graph theoretical analysis to analyze network topologies, we provide the first evidence for a maturational trajectory, throughout childhood and adolescence, for the recruitment of expressive language regions into large scale ensembles of coherently oscillating neurons.…”

Disrupted socio-emotional neural circuitry in adolescents with borderline personality traits

“…We selected this active time window based on previous research indicating differences in phase synchronization 0 -400 ms after stimulus presentation using the same task (29). NBS is a non-parametric technique to identify significant differences in network connectivity while controlling for family wise error rate (FWE; 37, 38).…”

“…The emotional faces task is described in Leung and colleagues (29). Angry and happy faces (25 faces, 13 males) with validity ratings of 0.8 proportion correct or higher were chosen from the MacBrain Face Stimulus Set (30) available at www.macbrain.org.…”