Cortical Correlates of Gustatory and Olfactory Avoidance in Autism

Background:  Autism spectrum disorder (ASD) has been linked with sensory related atypicalities dating back to seminal descriptions by Leo Kanner and Hans Asperger. This sensory dysfunction is thought to contribute to, if not drive feeding-related problems in ASD. These problems, including food selectivity and food refusal, are considerable mealtime stressors for families and interfere with daily functioning during adolescence and adulthood. Nevertheless, to date, investigations into sensory-related phenomena in ASD have concentrated on vision and audition to the relative exclusion of gustation and olfaction. Moreover, the neural underpinnings of taste and smell remain largely unexplored in ASD. Therefore, in the present study we investigated structural neural correlates of gustatory and olfactory sensory atypicalities in ASD.

Objectives:   Examine structural brain correlates of gustatory and olfactory avoidance in ASD.

Methods:   40 adolescent and young adult males with ASD (M age=16.60, SD=2.78; M IQ=113.28, SD=15.08), diagnosed using the Autism Diagnostic Interview, Autism Diagnostic Observation Schedule, and DSM criteria, completed self-ratings of items from the olfactory portion of the Sensory Avoidance quadrant of the Adolescent/Adult Sensory Profile. Each participant also provided a high-resolution 3 Tesla anatomic magnetic resonance imaging scan. The FreeSurfer image analysis suite (version 5.1) was used to derive vertex-level cortical thickness and to complete data analysis.

Results:   In the ASD group, increasing gustatory/olfactory avoidance was associated with increasing cortical thickness (cluster corrected ps<.05) in several regions, including the primary (insula and frontal operculum) and secondary (portions of the orbitofrontal cortex) gustatory cortex of the right hemisphere and both inferior and medial temporal cortices bilaterally. See Figure 1. 

Conclusions:   This is the first study to examine neural correlates of gustatory and olfactory avoidance in ASD. Strikingly, self-ratings of these behaviors in ASD were correlated with thickness in distinct cortical regions (e.g., insula/frontal operculum and orbitofrontal cortex) that are crucial to gustatory and olfactory function more broadly. These findings complement existing literature linking these sensory-related behaviors with these brain regions using structural brain imaging in non-ASD populations. For example, one prior study found increased cortical thickness in the orbitofrontal cortices and increased gray matter volume in medial temporal cortices in congenital anosmia (i.e., the loss of smell) (Frasnelli et al., 2013; NeuroImage). Another study found that individual differences in laboratory tests of olfactory function were positively associated with cortical thickness in the insula and orbitofrontal cortices of the right hemisphere in neurotypical adults (Frasnelli et al., 2010; Exp Brain Res). The present study extends this work to ASD, which is characterized by both gustatory and olfactory sensory avoidance. However, it remains unclear whether these brain correlates are the result of a history of these sensory-related avoidant behaviors or their cause. Future work in earlier developmental periods and longitudinal studies are needed to answer this question.