It’s All in the Eyes: Subcortical and Cortical Activation during Grotesqueness Perception in Autism

Abstract

Atypical face processing plays a key role in social interaction difficulties encountered by individuals with autism. In the current fMRI study, the Thatcher illusion was used to investigate several aspects of face processing in 20 young adults with high-functioning autism spectrum disorder (ASD) and 20 matched neurotypical controls. “Thatcherized” stimuli were modified at either the eyes or the mouth and participants discriminated between pairs of faces while cued to attend to either of these features in upright and inverted orientation. Behavioral data confirmed sensitivity to the illusion and intact configural processing in ASD. Directing attention towards the eyes vs. the mouth in upright faces in ASD led to (1) improved discrimination accuracy; (2) increased activation in areas involved in social and emotional processing; (3) increased activation in subcortical face-processing areas. Our findings show that when explicitly cued to attend to the eyes, activation of cortical areas involved in face processing, including its social and emotional aspects, can be enhanced in autism. This suggests that impairments in face processing in autism may be caused by a deficit in social attention, and that giving specific cues to attend to the eye-region when performing behavioral therapies aimed at improving social skills may result in a better outcome.

Face processing in autism spectrum disorders: From brain regions to brain networks

“…Kliemann et al (2012) found that the ASD group was marginally slower than NTs overall and also identified fewer expressions; however, both groups were fastest for happy expressions. Zürcher et al (2013) found that the NT group was more accurate overall, while both groups made more inverted face errors; the NT group made more inverted mouth errors and the ASD group made fewer upright eye errors. The ASD group was also faster for inverted faces.…”

“…The fMRI data demonstrate that forcing eye-region fixation in individuals with ASD tends to increase FG (Dalton et al, 2005; Perlman et al, 2011; Zürcher et al, 2013) and amygdala (Dalton et al, 2005; Kleinmann et al, 2012; Tottenham et al, 2013) activity, suggesting that face feature fixation manipulation can modulate and even normalize face sensitive cortical activity (Table 5). Although forced eye-fixation increases FG and amygdala activation in ASD, it is unclear if this provides support for either the active-avoidance or eye-area indifference theory.…”

“…Thus, low-level global processing deficits in ASD may hinder higher order ‘holistic’ face perception, while low-level motion processing deficits may hinder higher order gaze and expression biological motion processing (Berhmann et al, 2006). Face perception studies have found both disruption (Bird et al, 2006; Kleinhans et al, 2011; Zürcher et al, 2013) and preservation (Coutanche et al, 2011; Jiang et al, 2013; Pelphrey et al, 2007; von dem Hagen et al, 2014) of early visual processing stream cortical areas in individuals with ASD. These studies are reviewed in more detail below.…”

“…Paradigms exploring eye-fixation in ASD have utilized neutral (Zürcher et al, 2013) and emotional expressions (Dalton et al, 2005; Kliemann et al, 2012; Perlman et al, 2011; Tottenham et al, 2013) in tasks involving expression identification (Dalton et al, 2005; Kliemann et al, 2012), identity judgments of familiar family members (Dalton et al, 2005), identifying color changes of a fixation cross moving around the screen (Perlman et al, 2011), matching upright and inverted pairs of ‘Thacherized’ face stimuli (Zürcher et al, 2013), or identifying an object placed in the eye region of face stimuli (Tottenham et al, 2013). For example, Perlman et al (2011) used a moving fixation cross to force eye-fixation over various regions of the face, Kliemann et al (2012) moved the presentation of the face so that either the eye or mouth region randomly replaced the fixation cross on each trial, Zürcher et al (2013) randomly inverted the eye or mouth region while telling participants where to focus on each trial, and Tottenham et al (2013) randomly placed an opaque object in the left or right eye across trials.…”

“…For example, Perlman et al (2011) used a moving fixation cross to force eye-fixation over various regions of the face, Kliemann et al (2012) moved the presentation of the face so that either the eye or mouth region randomly replaced the fixation cross on each trial, Zürcher et al (2013) randomly inverted the eye or mouth region while telling participants where to focus on each trial, and Tottenham et al (2013) randomly placed an opaque object in the left or right eye across trials.…”