Neural correlates of taste reactivity in autism spectrum disorder

Jason A Avery, John E Ingeholm, Sophie Wohltjen, Meghan Collins, Cameron D Riddell, Stephen J Gotts, Lauren Kenworthy, Gregory L Wallace, W Kyle Simmons, Alex Martin, Jason A Avery, John E Ingeholm, Sophie Wohltjen, Meghan Collins, Cameron D Riddell, Stephen J Gotts, Lauren Kenworthy, Gregory L Wallace, W Kyle Simmons, Alex Martin

Abstract

Selective or 'picky' eating habits are common among those with autism spectrum disorder (ASD). These behaviors are often related to aberrant sensory experience in individuals with ASD, including heightened reactivity to food taste and texture. However, very little is known about the neural mechanisms that underlie taste reactivity in ASD. In the present study, food-related neural responses were evaluated in 21 young adult and adolescent males diagnosed with ASD without intellectual disability, and 21 typically-developing (TD) controls. Taste reactivity was assessed using the Adolescent/Adult Sensory Profile, a clinical self-report measure. Functional magnetic resonance imaging was used to evaluate hemodynamic responses to sweet (vs. neutral) tastants and food pictures. Subjects also underwent resting-state functional connectivity scans.The ASD and TD individuals did not differ in their hemodynamic response to gustatory stimuli. However, the ASD subjects, but not the controls, exhibited a positive association between self-reported taste reactivity and the response to sweet tastants within the insular cortex and multiple brain regions associated with gustatory perception and reward. There was a strong interaction between diagnostic group and taste reactivity on tastant response in brain regions associated with ASD pathophysiology, including the bilateral anterior superior temporal sulcus (STS). This interaction of diagnosis and taste reactivity was also observed in the resting state functional connectivity between the anterior STS and dorsal mid-insula (i.e., gustatory cortex).These results suggest that self-reported heightened taste reactivity in ASD is associated with heightened brain responses to food-related stimuli and atypical functional connectivity of primary gustatory cortex, which may predispose these individuals to maladaptive and unhealthy patterns of selective eating behavior.

Trial registration: (clinicaltrials.gov identifier) NCT01031407. Registered: December 14, 2009.

Keywords: Autism; Food; Insula; Superior temporal sulcus; Taste; fMRI.

Figures

Fig. 1
Fig. 1
Self-reported taste reactivity is related to the brain's response to sweet tastants in subjects with ASD. A. Within gustatory-responsive regions of left anterior and left mid insula (identified with a gustatory localizer), the response to sweet vs. neutral tastants in ASD subjects (but not TD controls) was positively related to a clinical measure of taste reactivity. B. A whole brain analysis of this relationship identified a host of brain regions associated with gustation, reward, and ASD pathophysiology exhibiting a positive relationship between taste reactivity and tastant response in ASD subjects. No similar relationships were observed in the analysis of TD subjects. AASP – Adolescent/Adult Sensory Profile; ASD - Autism Spectrum Disorder; TD – Typically Developing (control group); OFC – Orbitofrontal Cortex; ACC – Anterior Cingulate Cortex; PCC – Posterior Cingulate Cortex; STS – Superior Temporal Sulcus.
Fig. 2
Fig. 2
Brain regions exhibiting group differences in the relationship between taste reactivity and the response to food stimuli. A. Several brain regions (coronal and sagittal slices below) were identified in a whole-brain analysis examining the interaction of group (ASD vs. TD) by taste reactivity on the response to sweet vs. neutral tastants. B. (Left scatterplot) The beta weights, extracted and averaged across each of those brain regions, demonstrates the crossover interaction of tastant response by taste reactivity in ASD and TD groups. C. (Right scatterplot) A similar Region-Of-Interest (ROI) analysis using data from the Food Picture task demonstrates that these brain regions exhibit the same crossover interaction effect for the response to food vs. object pictures. AASP – Adolescent/Adult Sensory Profile; ASD - Autism Spectrum Disorder; TD – Typically Developing (control group).
Fig. 3
Fig. 3
Interactions of diagnosis and taste reactivity on the resting-state connectivity of the anterior superior temporal sulcus. We examined the seed-based connectivity of each of brain region that displayed a significant group by taste reactivity interaction of the response to food stimuli (see Fig. 2a). The bilateral anterior superior temporal sulcus (STS) exhibited a similar interaction in its resting-state connectivity to the bilateral dorsal mid-insular cortex. Scatterplots, included for display purposes only, show the direction of connectivity × taste reactivity relationships within 5 mm spheres around peak voxels in left and right mid-insula. AASP – Adolescent/Adult Sensory Profile; ASD - Autism Spectrum Disorder; TD – Typically Developing (control group).

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