A computational probe into the behavioral and neural markers of atypical facial emotion processing in autism

Abstract

Despite ample behavioral evidence of atypical facial emotion processing in individuals with autism (IwA), the neural underpinnings of such behavioral heterogeneities remain unclear. Here, I have used brain-tissue mapped artificial neural network (ANN) models of primate vision to probe candidate neural and behavior markers of atypical facial emotion recognition in IwA at an image-by-image level. Interestingly, the ANNs' image-level behavioral patterns better matched the neurotypical subjects' behavior than those measured in IwA. This behavioral mismatch was most remarkable when the ANN behavior was decoded from units that correspond to the primate inferior temporal (IT) cortex. ANN-IT responses also explained a significant fraction of the image-level behavioral predictivity associated with neural activity in the human amygdala, strongly suggesting that the previously reported facial emotion intensity encodes in the human amygdala could be primarily driven by projections from the IT cortex. Furthermore, in silico experiments revealed how learning under noisy sensory representations could lead to atypical facial emotion processing that better matches the image-level behavior observed in IwA. In sum, these results identify primate IT activity as a candidate neural marker and demonstrate how ANN models of vision can be used to generate neural circuit-level hypotheses and guide future human and non-human primate studies in autism.