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Hypersensitivity to low intensity fearful faces in autism when fixation is constrained to the eyes
Authors:Amandine Lassalle  Jakob Åsberg Johnels  Nicole R Zürcher  Loyse Hippolyte  Eva Billstedt  Noreen Ward  Eric Lemonnier  Christopher Gillberg  Nouchine Hadjikhani
Institution:1. Massachusetts General Hospital, A. Martinos Center for Biomedical Imaging, Harvard Medical School, Boston, Massachusetts, USA;2. Department of Psychiatry, Autism Research Centre, Cambridge University, United Kingdom;3. Gillberg Neuropsychiatry Center, Gothenburg University, Sweden;4. Section for Speech and Language Pathology, Gothenburg University, Sweden;5. Service de Génétique Médicale, University of Lausanne, Switzerland;6. Centre Ressource Autisme, Hopital Universitaire de Limoges, France
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.
Keywords:facial expressions  eye contact  autism  fMRI  amygdala  fear
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