Hypersensitivity to low intensity fearful faces in autism when fixation is constrained to the eyes

Abstract

Previous studies that showed decreased brain activation in people with autism spectrum disorder (ASD) viewing expressive faces did not control that participants looked in the eyes. This is problematic because ASD is characterized by abnormal attention to the eyes. Here, we collected fMRI data from 48 participants (27 ASD) viewing pictures of neutral faces and faces expressing anger, happiness, and fear at low and high intensity, with a fixation cross between the eyes. Group differences in whole brain activity were examined for expressive faces at high and low intensity versus neutral faces. Group differences in neural activity were also investigated in regions of interest within the social brain, including the amygdala and the ventromedial prefrontal cortex (vmPFC). In response to low intensity fearful faces, ASD participants showed increased activation in the social brain regions, and decreased functional coupling between the amygdala and the vmPFC. This oversensitivity to low intensity fear coupled with a lack of emotional regulation capacity could indicate an excitatory/inhibitory imbalance in their socio-affective processing system. This may result in social disengagement and avoidance of eye-contact to handle feelings of strong emotional reaction. Our results also demonstrate the importance of careful control of gaze when investigating emotional processing in ASD. Hum Brain Mapp 38:5943-5957, 2017. © 2017 Wiley Periodicals, Inc.

Facial Expression Processing Across the Autism–Psychosis Spectra: A Review of Neural Findings and Associations With Adverse Childhood Events

“…These results have been interpreted in light of the social motivation theory of ASD (100), suggesting that hypoactivity in the fusiform gyrus in the absence of guiding cues might reflect the lack of motivation to attend to salient expressive facial features (92). Similar effects have been reported for the amygdala, with enhanced amygdala activity when attention is oriented toward the eyes of the faces (92,107). In addition, modulatory effects of task demands on neural activation during facial expression perception have also been reported (91,92,94).…”

Pupillary Contagion in Autism

“…increased arousal levels during socioaffective processing. Although we acknowledge the associational nature of that finding, the results are clearly in line with such a proposal (Lassalle et al, 2017), whereas they are difficult to reconcile with theories postulating a pervasive insensitivity or indifference to socioaffective stimuli in individuals with ASD (Chevallier et al, 2012;Kanner, 1944). Potential weaknesses of this work are the limited number of emotional expressions, the number of trials within each condition, and the use of static as opposed to dynamic presentation of the pupils.…”

“…Heightened arousal may also explain the social disengagement that characterizes autism at the behavioral level. According to overarousal hypotheses, such as the socioaffective-excitatory/inhibitory-imbalance model (Lassalle et al, 2017), the avoidance of social stimuli, including eye gaze, is not an index of indifference to other individuals but a coping mechanism to downregulate high arousal levels (cf. Dalton et al, 2005).…”

Impairments in cognitive empathy and alexithymia occur independently of executive functioning in college students with autism

“…Impairments in empathy have been reported in both children and adults with ASD (Auyeung et al, 2009;Sucksmith et al, 2013), as well as for ASD individuals with high levels of intelligence (IQ; Baron- Cohen and Wheelwright, 2004;Lombardo et al, 2007). Interestingly, the empathy imbalance hypothesis (EIH) of autism (Smith, 2009) suggests that, instead of a global empathy deficit, only cognitive empathy is compromised in individuals with ASD and the capacity for affective empathy is heightened, as indicated by hyperarousal in response to emotional cues by others, such as fearful facial expressions (Lassalle et al, 2017). A specific deficit in cognitive empathy has been supported recurrently by studies in individuals with ASD, with and without high IQ (Bellebaum et al, 2014;Dziobek et al, 2008;Frith, 2001;Lockwood et al, 2013;Pouw et al, 2013;Rogers et al, 2007).…”