Atypical Functional Network Connectivity to Emotional Faces in Adults with ASD

Background:

Pronounced socio-emotional impairments, including atypical emotional face processing, are inherent to autism spectrum disorder (ASD). At the neural level, differences in functional networks during face processing in ASD compared to controls have been highlighted recently (Kana et al., 2016), which may be associated with difficulties in social functioning. However, few studies have used magnetoencephalography (MEG) to investigate functional connectivity during affective processing in ASD. MEG is ideally suited to examine functional connectivity - it is a direct measure of neural activity and offers good spatial and excellent temporal resolution.

Objectives:

We investigated whole-brain functional connectivity using MEG in the largest sample to date of adults with ASD 48 (M_age= 26.76, SD= 5.21) and 60 typical developed age-matched controls (M_age= 26.64, SD= 5.87) during the implicit presentation of emotional faces.

Methods:

Adults participated in an emotional faces task, in which each trial consisted of a happy or angry face and a scrambled pattern (target stimulus) simultaneously presented for 80ms on either side of a central fixation cross. Participants indicated the location of the target (left or right) as rapidly as possible by pressing a button. Structural MRIs were obtained for MEG co-registration. MEG data were epoched by emotional face type. Time series were estimated from 90 cortical and subcortical sources of the AAL atlas using the LCMV beamformer. The phase-lag index was used to assess phase synchronization of ongoing neural oscillations among sources (Stam, Nolte & Daffertshofer, 2007).

Results:

We found a network of increased beta-band phase synchrony 58-228ms following angry faces in adults with ASD compared to controls (35 edges, 35 nodes; p_corr= 0.019). This network involved almost exclusively connections among bilateral frontal, including orbitofrontal areas and the right ACC, and temporal regions, including left superior temporal gyrus. Additionally, reduced phase synchrony in the low-gamma frequency band 85-283ms following angry face onset was found in the adults with ASD (51 edges, 47 nodes; p_corr< 0.001). This network was anchored in frontal regions, including orbitofrontal areas and the right ACC, and connecting to occipital, and temporal regions, also including the right amygdala.

Conclusions:

These results indicate atypical patterns of hyper- and hypo-connectivity during angry face processing in the beta and low-gamma frequency bands in adults with ASD compared to typical controls. The current findings may suggest atypical top-down/bottom-up functional connectivity in ASD. In particular, beta-band synchronization is implicated in top-down influences, while gamma-band synchronization is involved in bottom-up influences (Fries, 2015). In the current study, greater beta-band phase synchrony may suggest increased top-down influences from primarily frontal areas in adults with ASD compared to controls, whereas reduced gamma phase synchrony may suggest lower bottom-up influences of regions, including the amygdala, which may contribute to difficulties with selective attention of emotional faces in ASD. Abnormal top-down functional connectivity has recently been proposed in this population (Mamashli et al., 2018). Overall, findings are consistent with previous work reporting abnormal neurodevelopment of functional connectivity to emotional faces in ASD (Mennella et al., 2018; Safar et al., 2018).