Elsevier

Biological Psychology

Volume 149, January 2020, 107774
Biological Psychology

Emotional face processing in autism spectrum disorder: Effects in gamma connectivity

https://doi.org/10.1016/j.biopsycho.2019.107774Get rights and content

Highlights

  • MEG used to examine functional connectivity to emotional faces in ASD and controls.

  • Reduced gamma phase synchrony during angry perception was found in adults with ASD.

  • This network involved widespread connections anchored in frontal regions.

  • Gamma band-specific disrupted neural circuitry may reflect altered E/I balance in ASD.

  • This disrupted network may underlie abnormal processing of angry faces in ASD.

Abstract

Impairments in social functioning are characteristic of autism spectrum disorder (ASD). Differences in functional networks during face processing in ASD compared to controls have been reported; however, the spatial-temporal dynamics of networks underlying affective processing are still not well understood. The current magnetoencephalography study examined whole-brain functional connectivity to implicit happy and angry faces in 104 adults with and without ASD. A network of reduced gamma band (30–55 Hz) phase synchrony occurring 80–308 ms following angry face presentation was found in adults with ASD compared to controls. The network involved widespread connections primarily anchored in frontal regions, including bilateral orbitofrontal areas, bilateral inferior frontal gyri, and left middle frontal gyrus extending to occipital, temporal, parietal, and subcortical regions. This finding suggests disrupted long-range neuronal communication to angry faces. Additionally, reduced gamma band-specific connectivity may reflect altered E/I balance in brain regions critical for emotional face processing in ASD.

Introduction

Pronounced socio-emotional impairments, such as atypical emotional face processing, are inherent to autism spectrum disorder (ASD; American Psychiatric Association, 2013). Emotional face processing involves widespread brain areas, such as right occipital temporal and parietal cortices and bilateral amygdalae, insular cortices, and frontal areas (i.e., orbitofrontal, medial prefrontal and anterior cingulate cortices; ACC; Adolphs, 2002; Haxby, Hoffman, & Gobbini, 2002); many of these brain areas are activated atypically in ASD (Harms, Martin, & Wallace, 2010).

Task-based functional connectivity studies using functional magnetic resonance imaging (fMRI) have highlighted differences in functional networks during face and emotional face processing in ASD relative to controls (Kana, Patriquin, Black, Channell, & Wicker, 2015; Kleinhans et al., 2008; Monk, 2010; Rudie et al., 2011; Sato, Toichi, Uono, & Kochiyama, 2012; Welchew et al., 2005; Wicker et al., 2008). For instance, Kana et al. (2015) observed a network of reduced functional connectivity in ASD among the medial prefrontal cortex and other key emotion processing regions, including the amygdalae, temporal and parietal lobes, and fusiform gyri (FG) during implicit emotion processing. The authors suggested that given implicit emotion processing is automatic and rapid, this ability may be particularly impaired in those with ASD.

The more recent use of magnetoencephalography (MEG) to study task-based functional connectivity in ASD has extended our understanding of the spatial-temporal dynamics of functional networks in this population, greatly complementing haemodynamic approaches. A small number of MEG studies have reported atypical interregional differences in phase synchrony of neural oscillations (an index of functional connectivity and fundamental to coordinating information among neural networks supporting socio-cognitive processes; Fries, 2005; Stam, Nolte, & Daffertshofer, 2007), to emotional faces in ASD. Using MEG, Safar, Wong, Leung, Dunkley, and Taylor (2018)) examined whole-brain phase synchrony of eight a priori regions of interest (i.e., bilateral amygdalae, FG, insulae and ACC) during an implicit emotional faces task in 20 children with ASD and 22 typically developing controls between the ages of 7 and 10 years. They found increased alpha band phase synchrony 0–400 ms following happy face perception in children with ASD compared to controls in a network involving key emotion processing areas, such as the bilateral orbitofrontal cortices, right inferior frontal gyrus, left FG, right superior temporal gyrus and right insula. Additionally, alpha band connectivity strength of the left FG and right insula was greater in children with ASD than controls, suggesting that these two regions were more strongly connected in whole-brain analyses in ASD than controls during happy face processing. Similarly using MEG and the same task, Leung, Ye, Wong, Taylor, and Doesburg (2014) examined whole-brain phase synchrony during implicit happy and angry face perception in 22 adolescents with and 17 without ASD. Adolescents with ASD demonstrated a network of reduced interregional beta band phase synchrony during the first 400 ms of angry face processing compared to adolescent controls, which importantly involved the bilateral insulae, right supramarginal gyrus and right FG, as well as frontal brain regions, including the left middle frontal gyrus, right superior frontal gyri and left inferior frontal gyrus. Furthermore, the right insula was the hub of reduced beta-band connectivity strength, eigenvector centrality, and clustering. These results were interpreted to reflect disrupted communication and atypical recruitment of brain regions typically part of socio-emotional circuitry in ASD. Using the same task in adults with ASD and controls (n = 22 in each group), Mennella, Leung, Taylor, & Dunkley (2017) found that similar to adolescents with ASD, adults with ASD also showed reduced whole-brain beta band phase synchrony around 300 ms following the presentation of angry faces compared to controls. This hyposynchronous network involved predominantly connections among frontal, limbic and occipital areas. Interestingly, the left amygdala, left insula and striatum, which play a key role in affective processing, were underconnected in this network (Mennella et al., 2017).

Overall, MEG studies have highlighted networks of atypical functional neural circuitry during implicit happy and angry face processing in ASD at different developmental periods, which suggests altered maturation of neural networks underpinning socio-emotional processing in this population; however, a limitation of the above work is the relatively small sample sizes of ASD and control groups. Given the heterogeneity in ASD (O’Reilly, Lewis, & Elsabbagh, 2017), it is essential to investigate neural networks involved in emotion processing in larger groups. The current study used MEG to investigate whole-brain functional connectivity in a sample of adults with ASD and age- and sex-matched controls (n = 104) during the implicit perception of happy and angry faces. Based on few studies reporting reduced functional connectivity during angry face processing in adolescents and adults using MEG (Khan et al., 2013; Leung et al., 2014; Mennella et al., 2017), we hypothesized that adults with ASD would show reduced functional connectivity during the implicit processing of angry faces compared to controls. We did not expect group differences in functional connectivity to happy faces.

Section snippets

Participants

One hundred and four subjects were included in the analysis: 44 adults with ASD (M age = 26.5 years, SD = 5.99, range = 18.5–39.5 years, 32 males, 80% right-handed) and 60 age- and sex-matched controls (M age = 26.6 years, SD = 5.21, range = 18.5–38.8 years, 40 males, 88% right-handed). A subset of adults with ASD (n = 18) and controls (n = 19) were included in Mennella et al. (2017). Data from 25 additional participants (n = 15 ASD) were excluded from the analysis due to excessive artefacts

Behavioural results

For measures of reaction time (ms) and accuracy (percent correct), we calculated Mann-Whitney U tests due to non-normality of the distributions for both happy and angry faces. Adults with and without ASD performed comparably in their reaction times to happy U = 1260, z = -0.395, p = 0.693 and angry faces U = 1278, z = -0.276, p =  0.782. Similarly, for accuracy, no significant group differences were found for happy U = 1543.5, z = 1.5, p = 0.135, or angry faces U = 1472.5, z = 1.021, p = 0.307

Discussion

The current study investigated whether functional connectivity is disrupted during the implicit perception of emotional faces in a large sample of adults with and without ASD. We found a network of reduced gamma band phase synchrony 80–308 ms following angry face onset in adults with ASD compared to controls. This hyposynchronous network in MEG primarily involved connections among frontal regions and occipital and occipitotemporal regions, including the left calcarine, right middle occipital

Declaration of Competing Interest

All authors have no declarations of interest to report.

Acknowledgments

Funding: This work was supported by the Canadian Institutes of Health Research (CIHR) [MOP-119541; MOP-142379].

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