Prefrontal Responses to Odors in Individuals With Autism Spectrum Disorders: Functional NIRS Measurement Combined With a Fragrance Pulse Ejection System.

Mingdi Xu,Nozomi Naoi,Hirokazu Kumazaki,Ken-Ichi Okada,Yasuyo Minagawa

doi:10.3389/fnhum.2020.523456

Abstract

Individuals with autism spectrum disorders (ASD) are impaired not only in social competencies but also in sensory perception, particularly olfaction. The olfactory ability of individuals with ASD has been examined in several psychophysical studies, but the results have been highly variable, which might be primarily due to methodological difficulties in the control of odor stimuli (e.g., the problem of lingering scents). In addition, the neural correlates of olfactory specificities in individuals with ASD remain largely unknown. To date, only one study has investigated this issue using functional magnetic resonance imaging (fMRI). The present study utilized a sophisticated method−a pulse ejection system−to present well-controlled odor stimuli to participants with ASD using an ASD-friendly application. With this advantageous system, we examined their odor detection, identification, and evaluation abilities and measured their brain activity evoked by odors using functional near-infrared spectroscopy (fNIRS). As the odor detection threshold (DT) of participants with ASD was highly variable, these participants were divided into two groups according to their DT: an ASD-Low DT group and an ASD-High DT group. Behavioral results showed that the ASD-High DT group had a significantly higher DT than the typically developing (control) group and the ASD-Low DT group, indicating their insensitivity to the tested odors. In addition, while there was no significant difference in the odor identification ability between groups, there was some discrepancy between the groups’ evaluations of odor pleasantness. The brain data identified, for the first time, that neural activity in the right dorsolateral prefrontal cortex (DLPFC) was significantly weaker in the ASD-High DT group than in the control group. Moreover, the strength of activity in the right DLPFC was negatively correlated with the DT. These findings suggest that participants with ASD have impairments in the higher-order function of olfactory processing, such as olfactory working memory and/or attention.

Highlights

Individuals with autism spectrum disorders (ASD) generally have unusual sensory awareness, showing either hyper- or hyporesponsiveness to various sensory modalities, including olfaction (Kientz and Dunn, 1997; Rogers et al, 2003; Rogers and Ozonoff, 2005; Schreck and Williams, 2006; Ben-Sasson et al, 2009; Wiggins et al, 2009)
According to the virtual registration method (Tsuzuki et al, 2007), multiple channels covering the dorsolateral prefrontal cortex (DLPFC) were activated in the control group (CH9, right DLPFC 100%; CH10, left DLPFC 91.7%, frontal pole (FP) 8.3%; CH13, right DLPFC 78.9%, FP 21.1%; FIGURE 4 | Performance of participants with ASD and typically developing (TD) control participants in the (A) odor detection threshold (DT), (B) odor identification, and (C) odor evaluation tests
The strength of olfaction-evoked neural activity in the right DLPFC was correlated with DT

Summary

Introduction

Individuals with autism spectrum disorders (ASD) generally have unusual sensory awareness, showing either hyper- or hyporesponsiveness to various sensory modalities, including olfaction (Kientz and Dunn, 1997; Rogers et al, 2003; Rogers and Ozonoff, 2005; Schreck and Williams, 2006; Ben-Sasson et al, 2009; Wiggins et al, 2009). Some studies suggested preserved odor sensitivity in individuals with ASD (Suzuki et al, 2003; Tavassoli and BaronCohen, 2012; Galle et al, 2013; Addo et al, 2017), whereas other studies reported either enhanced (Ashwin et al, 2014) or decreased odor sensitivity (Dudova et al, 2011; Kumazaki et al, 2016). While Kumazaki et al (2019) demonstrated decreased odor adaptation in children with ASD as compared to TD children, Tavassoli and Baron-Cohen (2012) reported similar odor adaptation in adults with ASD and TD adults This is in contrast to the well-established literature on abnormalities in vision (Simmons et al, 2009), audition (O’Connor, 2012), and touch (Puts et al, 2014) in individuals with ASD

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