The Role of the Amygdala in Atypical Gaze on Emotional Faces in Autism Spectrum Disorders

Abstract

Reduced focus toward the eyes is a characteristic of atypical gaze on emotional faces in autism spectrum disorders (ASD). Along with the atypical gaze, aberrant amygdala activity during face processing compared with neurotypically developed (NT) participants has been repeatedly reported in ASD. It remains unclear whether the previously reported dysfunctional amygdalar response patterns in ASD support an active avoidance of direct eye contact or rather a lack of social attention. Using a recently introduced emotion classification task, we investigated eye movements and changes in blood oxygen level-dependent (BOLD) signal in the amygdala with a 3T MRI scanner in 16 autistic and 17 control adult human participants. By modulating the initial fixation position on faces, we investigated changes triggered by the eyes compared with the mouth. Between-group interaction effects revealed different patterns of gaze and amygdalar BOLD changes in ASD and NT: Individuals with ASD gazed more often away from than toward the eyes, compared with the NT group, which showed the reversed tendency. An interaction contrast of group and initial fixation position further yielded a significant cluster of amygdala activity. Extracted parameter estimates showed greater response to eyes fixation in ASD, whereas the NT group showed an increase for mouth fixation.The differing patterns of amygdala activity in combination with differing patterns of gaze behavior between groups triggered by direct eye contact and mouth fixation, suggest a dysfunctional profile of the amygdala in ASD involving an interplay of both eye-avoidance processing and reduced orientation.

Linking social behaviour and anxiety to attention to emotional faces in Williams syndrome

“…These links have however been made in studies investigating gaze patterns in ASD. Indeed, diminished fixation to the eye region has been associated with greater levels of social anxiety in ASD independent of autism severity (Corden, Chilvers, & Skuse, 2008) as well as amygdala hyper-responsiveness (Dalton et al, 2005;Kliemann et al, 2012). Interestingly, the atypical gaze patterns away from threatening eyes did not result in poorer recognition of fearful or angry faces in our WS group relative to their developmental level, providing the preliminary suggestion that gaze away from this region may be more related to the effects of enhanced arousal than reduced attention to the eye region.…”

“…Thirdly, we aimed to explore the relationship between behavioural aspects of anxiety and reciprocal social behaviour and attentional allocation to emotional expressions and face regions in WS. On the basis of previous studies showing that anxiety mediates amygdala response to direct eye gaze to threatening faces in ASD (Kliemann, Dziobek, Hatri, Baudewig, & Heekeren, 2012), we expected that individuals with WS who display higher levels of anxiety and social reciprocity difficulties would show reduced attention to the eye region of threatening facial expressions.…”

Violations of Personal Space in Young People with Autism Spectrum Disorders and Williams Syndrome: Insights from the Social Responsiveness Scale

“…Kennedy et al (2009) (Kliemann et al, 2012). Therefore, it remains speculative as to whether interpersonal distance regulation could be an endophenotype for amygdala dysfunction in WS and ASD (Kennedy & Adolphs, 2014).…”

Appearance-based trust behaviour is reduced in children with autism spectrum disorder

“…Their perceptions of trustworthiness have received particular attention, because these judgments have been linked with the functioning of the amygdala (Adolphs, Sears and Piven, 2001;Winston, Strange, O'Doherty and Dolan, 2004), which may be atypical in ASD (Ashwin, Baron-Cohen, Wheelright, O'Riordan and Bullmore, 2007;Critchley et al, 2000;Kliemann, Dziobek, Hatri, Baudewig and Heekeren, 2012).…”