Atypical Predictive Processing Is Associated With Sensory Over-Responsivity in Autism

Abstract

Autism is characterized by sensory processing atypicalities including sensory over-responsivity (SOR), a heightened negative response to sensory stimuli. Although the neural mechanisms underlying SOR are not fully understood, SOR has been associated with sensory-limbic hyper-reactivity during sensory stimulation. Altered predictive processing may play a key role in atypical sensory processing but few studies have directly probed the relationship between SOR and prediction, particularly using aversive stimuli that bother autistic individuals in everyday life. Here, we examined whether visual cues signaling the onset of aversive sensory stimuli would either (a) reduce neural hyper-reactivity in autism by making stimuli less unexpected or (b) show limited effects in autism due to atypical predictive processing hindering the use of the cue to attenuate responses. Fifty-five autistic (ASD; 30 female, mean age 21.01 ± 3.49) and 28 typically developing (TD; 16 female, mean age 19.76 ± 3.00) adolescents and young adults underwent functional magnetic resonance imaging (fMRI) while they were exposed to mildly aversive auditory and tactile stimulation. Stimulus blocks were either presented with a visual cue representing the upcoming sensory stimulus (Predictable), or no cue (Unpredictable). Results showed sensory cortical hyper-reactivity in ASD compared to TD in the Unpredictable condition, but responses to Predictable stimuli were overall similar between groups. In addition, expected stimuli were associated with increased frontal activity in autism, suggesting that visual cues facilitated regulation of sensory responses. Notably, within the autism group, SOR was associated with increased responses to expected stimuli in relevant sensory cortices, suggesting that reduced expectancy suppression may be specifically related to SOR within ASD rather than being a general autistic trait.