Salience Network Connectivity Is Related to Brain and Behavioral Markers of Sensory over-Responsivity in ASD

Background: Children with autism spectrum disorders (ASD) often exhibit sensory over-responsivity (SOR), which may cause them to react negatively to sensory stimuli such as noisy environments or scratchy clothing (Liss et al., 2006), and SOR is associated with increased functional impairment  (e.g., Liss et al., 2006; Pfeiffer et al., 2005). Previous research from our lab suggests that SOR may be related to an overattribution of salience to extraneous sensory information, as individuals with ASD and SOR have hyperactivation and reduced habituation in the amygdala and sensory cortices in response to mildly aversive sensory stimuli (Green et al., 2015).  The salience network, an intrinsic brain network which is thought to modulate attention to internal versus external stimuli, has been consistently found to be atypical in ASD (Uddin et al., 2013). Salience network abnormalities during resting-state are thought to underlie some of the difficulties intrinsic to ASD, such as atypical allocation of attention to extraneous sensory stimuli rather than relevant social stimuli (Uddin et al., 2013). However, to-date there is little research on how differences in salience network organization in ASD relates to differences in brain function during information processing. Thus, in the present study we sought to examine how intrinsic connectivity in the salience network relates to SOR by integrating resting-state fMRI, task-based fMRI, and behavioral data.

Objectives: To examine how connectivity with the salience network (with anterior insula as the hub) during resting state relates to symptoms of SOR and to brain response to mildly aversive sensory stimuli.

Methods: Participants were 28 children and adolescents with ASD and 33 TD matched controls, between 8-17 years of age.  Children underwent a 6-minute resting-state scan as well as a separate fMRI paradigm, where they were presented with simultaneous mildly aversive auditory stimuli (noisy traffic sounds) and tactile stimuli (scratchy sweater rubbed from wrist to elbow). Parents completed the tactile, auditory, and visual scales of the Short Sensory Profile (REF) and SenSOR Invenstory (REF) and scores were standardized and combined into an SOR composite. Whole-brain connectivity with a 5-mm spherical seed in the right anterior insula (AI) was examined, with SOR composite scores as a regressor to determine resting state connectivity as a function of SOR severity. Correlations between resting-state salience network connectivity and brain response to mildly aversive tactile and auditory stimuli were examined.

Results: SOR in youth with ASD was related to increased resting-state functional connectivity between salience network nodes and brain regions implicated in primary sensory processing and attention (somatosensory cortex and amygdala). Further, the strength of this connectivity at rest was related to the extent of brain activity in these same areas in response to auditory and tactile stimuli.

Conclusions: Results support an association between intrinsic brain connectivity and specific atypical brain responses during information processing. Additionally, findings suggest that basic sensory information is overly salient to individuals with SOR, leading to over-attribution of attention to this information. Clinical implications include incorporating sensory coping strategies into social interventions for individuals with SOR.