We monitored regional cerebral blood volume changes using a 52-channel NIRS apparatus over the prefrontal cortex (PFC) and superior temporal sulcus (STS), 2 areas implicated in social cognition and the pathology of ASD, in 28 typically developed participants (14 male and 14 female) during face-to-face conversations. This task was designed to resemble a realistic social situation. We examined the correlations of these changes with autistic traits assessed using the Autism-Spectrum Quotient (AQ).

Autism spectrum disorders (ASD) are characterized by impaired social interaction and communication, restricted interests, and repetitive behaviours. The severity of these characteristics is posited to lie on a continuum that extends into the general population. Brain substrates underlying ASD have been investigated through functional neuroimaging studies using functional magnetic resonance imaging (fMRI). However, fMRI has methodological constraints for studying brain mechanisms during social interactions (for example, noise, lying on a gantry during the procedure, etc.). In this study, we investigated whether variations in autism spectrum traits are associated with changes in patterns of brain activation in typically developed adults. We used near-infrared spectroscopy (NIRS), a recently developed functional neuroimaging technique that uses near-infrared light, to monitor brain activation in a natural setting that is suitable for studying brain functions during social interactions.

Funding: Gunma University (Drs. Fukuda and Mikuni) and the Hitachi Group (Advanced Research Laboratory, Hitachi Ltd, and the Research and Developmental Center, Hitachi Medical Corporation) have had an official contract for a collaborative study of the clinical application of near-infrared spectroscopy in psychiatric disorders since 2002. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Introduction

Autism is a developmental disorder characterized by impaired social interactions and communication in addition to restricted and repetitive behaviour. In recent years, the concept of autism spectrum disorders (ASD) has been proposed; it hypothesizes a wide range of symptoms resembling autism, such as those demonstrated in Asperger syndrome and pervasive developmental disorder not otherwise specified. According to this concept, disorders across the spectrum are believed to have common biological bases. Postmortem and structural magnetic resonance imaging (MRI) studies have highlighted the prefrontal cortex (PFC), including the medial PFC, the superior temporal sulcus (STS), the amygdala, the anterior cingulate cortex, the fusiform gyrus, the thalamus, and the cerebellum as pathological substrates for ASD [1].

Many functional neuroimaging studies of ASD focusing on impaired social interactions and communication have been conducted using functional MRI (fMRI). By employing task stimuli related to social cognitive modules, such as face recognition, visual motion processing, the theory of mind, and eye-gaze perception, these studies have implicated several brain regions in the pathogenesis of autism, including the STS and the fusiform gyrus for face processing [2], [3]; the PFC, including the medial prefrontal cortex, for mentalising and person perception [4], [5]; the temporoparietal junction [6]; and the amygdala for threat detection, emotion recognition, and complex social judgments [7], [8]. Moreover, these studies have provided a foundation for understanding neural mechanisms underlying social deficits in ASD. However, fMRI has methodological constraints for studying brain mechanisms underlying social cognition. For example, participants are required to lie on a bed in a small, noisy gantry during examination, a condition that is upsetting to many people, including those with autism. Due to this limitation, most previous studies have necessarily been conducted in an unusual and unrealistic way, such as using pictures or computer graphics images shown on a computer monitor as task stimuli. A functional brain imaging methodology that enables monitoring of brain activation in a more natural setting might well offer more informative data from more realistic social interactive situations, such as having an interview with another person, which is impossible with fMRI because of its methodological constraints.

Near-infrared spectroscopy (NIRS) is a recently developed functional brain imaging technique that involves emission of near-infrared light that can be detected through the scalp [9]. NIRS allows monitoring of cerebral blood volume (CBV) changes in the neocortex as indicated by increased oxygenated haemoglobin concentrations ([oxy-Hb]) and decreased deoxygenated haemoglobin concentration ([deoxy-Hb]) using a small apparatus, although certain measurement concerns remain, such as the effect of blood flow in the scalp or the difficulty in determining the exact length of the light path for each subject. NIRS has some methodological limitations as well, such as a low spatial resolution (approximately 3 cm, which is nearly equal to 1 gyrus of the brain) and an inability to assess deep brain structures. Nevertheless, when an NIRS probe is placed on the head in one of the 10–20 standard electroencephalography electrode positions, the cerebrocranial correlation is considered to vary within 1 cm; therefore, correspondence at the level of the gyrus is not affected [10].

Despite these methodological limitations, NIRS enables brain activity measurement in a more natural setting compared with other functional brain imaging techniques. Subjects can undergo NIRS examination in a seated position, with their eyes open, while speaking, and without any noise or pain. These characteristics of NIRS are considered to be particularly suitable for social interaction studies. Thus far, NIRS has successfully been demonstrated for monitoring brain function in healthy participants during delicate and/or subjective experiences, such as subjective sleepiness and psychological fatigue [11], [12] and in patients with psychiatric disorders who are sensitive to the experimental environment [13]–[16]. In short, NIRS has certain distinct advantages, such as complete non-invasiveness, lack of restriction of body movement, and the small size of the apparatus, but it is not able to detect signals within the deep brain structure and has a low spatial resolution of approximately 1 gyrus.

In this study, we used NIRS to monitor brain activation in healthy seated participants during conversations to examine social cognition in a natural setting. Such an approach may further our understanding of brain activity during social interactions in everyday life and of associations between multiple social cognitive modules in realistic situations. We further investigated the relationship between brain activation in the PFC and STS regions during face-to-face conversations and, because the severity of characteristics of ASD is posited to lie on a continuum that extends into the general population, we evaluated autistic traits in typically developed adults [17], [18]. To determine the extent to which adults of average intelligence display characteristics associated with ASD, Baron-Cohen et al. developed a self-administered questionnaire, the Autism-Spectrum Quotient (AQ) [19]. We hypothesized that face-to-face conversations would activate the PFC as well as the STS (since both areas are involved in social cognition) and that variations in autistic traits in the typically developed participants would be correlated with brain activation during face-to-face conversations.