Sensory over-Responsivity and Social Cognition in ASD: Effects of Aversive Sensory Stimuli and Attentional Modulation on Neural Responses to Social Cues

Background: Sensory over-responsivity (SOR) is an impairing condition manifested as extreme sensitivity to stimuli such as unexpected loud noises or being touched. SOR is particularly common (rates of 56-70%) in autism spectrum disorders (ASD) and, notably, it is associated with higher impairment including greater deficits in social and adaptive behavior (Ben-Sasson et al., 2008). Although SOR is strongly linked to impairment, the mechanisms through which it disrupts social functioning are not well understood. Previous research from our lab suggests that SOR may be related to an overattribution of salience to extraneous sensory information. Individuals with ASD and SOR show hyperactivation and reduced habituation in the amygdala and sensory cortices in response to mildly aversive sensory stimuli (Green et al., 2015), as well as increased salience network connectivity with amygdala and somatosensory cortex (Green et al., 2016). Taken together, these studies suggest that SOR is associated with atypical allocation of attention to extraneous sensory stimuli rather than relevant social stimuli. Yet, the effect of sensory distracters on the brain’s ability to process social information has not been tested directly.

Objectives: To examine the effect of a tactile sensory distracter on brain responses during a social cognition task, and to test whether explicitly directing attention to relevant social cues can mitigate the effect of the sensory distracter.

Methods: Participants were 15 children and adolescents with ASD and 16 TD matched controls, between 8-17 years of age. While undergoing fMRI, children completed a social cognition task, which involved determining whether a speaker was sarcastic or sincere. They completed the task with/without a tactile sensory distracter, and with/without instructions directing their attention to relevant social cues. Parents completed the tactile scales of the Short Sensory Profile (Dunn, 1999) and SenSOR Inventory (Schoen et al., 2008); scores were combined into a tactile SOR composite.

Results: When completing the task in the presence of the sensory distracter, TD youth showed increased activity in auditory language and frontal regions whereas ASD youth showed decreased activation in these areas. Instructions mitigated this effect such that ASD youth no longer showed decreased activation during tactile stimulation; instead, the ASD group showed increased medial prefrontal (mPFC) activity. With attentional instructions, higher SOR was associated with greater activity in primary auditory and visual cortex as well as higher-level language and face processing regions, whereas lower SOR was associated with greater activity in temporal pole and mPFC, regions associated with integrative social cognition such as inference and theory of mind.

Conclusions: Results demonstrate for the first time a neural mechanism through which sensory stimuli may disrupt social cognition, and that attentional modulation can restore neural processing of social cues through prefrontal regulation. Attentional modulation may work through different mechanisms depending on level of SOR: youth with high SOR may rely on processing individual visual and auditory stimuli whereas youth with low SOR may be better able to integrate and interpret multiple social cues. Findings have implications for novel, integrative interventions that incorporate attentional directives to target both sensory and social symptoms.